Environmentally

Sustainable
Livestock
Production
Edited by
Ilkka Leinonen
Printed Edition of the Special Issue Published in Sustainability

www.mdpi.com/journal/sustainability
Environmentally Sustainable Livestock
Production
Environmentally Sustainable Livestock
Production

Special Issue Editor

Ilkka Leinonen

MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade

Special Issue Editor
Ilkka Leinonen
Scotland’s Rural College
UK

Editorial Office
MDPI
St. Alban-Anlage 66
4052 Basel, Switzerland

This is a reprint of articles from the Special Issue published online in the open access journal
Sustainability (ISSN 2071-1050) from 2018 to 2019 (available at: https://www.mdpi.com/journal/
sustainability/special issues/Environmentally Sustainable Livestock Production)

For citation purposes, cite each article independently as indicated on the article page online and as
indicated below:

LastName, A.A.; LastName, B.B.; LastName, C.C. Article Title. Journal Name Year, Article Number,
Page Range.

ISBN 978-3-03897-552-6 (Pbk)

ISBN 978-3-03897-553-3 (PDF)


c 2019 by the authors. Articles in this book are Open Access and distributed under the Creative
Commons Attribution (CC BY) license, which allows users to download, copy and build upon
published articles, as long as the author and publisher are properly credited, which ensures maximum
dissemination and a wider impact of our publications.
The book as a whole is distributed by MDPI under the terms and conditions of the Creative Commons
license CC BY-NC-ND.
Contents

About the Special Issue Editor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii

Preface to ”Environmentally Sustainable Livestock Production” . . . . . . . . . . . . . . . . . . ix

Ilkka Leinonen
Achieving Environmentally Sustainable Livestock Production
Reprinted from: Sustainability 2019, 11, 246, doi:10.3390/su11010246 . . . . . . . . . . . . . . . . . 1

Nathan Pelletier, Maurice Doyon, Bruce Muirhead, Tina Widowski, Jodey Nurse-Gupta and
Michelle Hunniford
Sustainability in the Canadian Egg Industry—Learning from the Past, Navigating the Present,
Planning for the Future
Reprinted from: Sustainability 2018, 10, 3524, doi:10.3390/su10103524 . . . . . . . . . . . . . . . . 6

Nathan Pelletier
Social Sustainability Assessment of Canadian Egg Production Facilities: Methods, Analysis, and
Recommendations
Reprinted from: Sustainability 2018, 10, 1601, doi:10.3390/su10051601 . . . . . . . . . . . . . . . . 30

Tianyi Cai, Degang Yang, Xinhuan Zhang, Fuqiang Xia and Rongwei Wu
Study on the Vertical Linkage of Greenhouse Gas Emission Intensity Change of the Animal
Husbandry Sector between China and Its Provinces
Reprinted from: Sustainability 2018, 10, 2492, doi:10.3390/su10072492 . . . . . . . . . . . . . . . . 47

Erasmus K.H.J. zu Ermgassen, Melquesedek Pereira de Alcântara, Andrew Balmford,

Luis Barioni, Francisco Beduschi Neto, Murilo M. F. Bettarello, Genivaldo de Brito,
Gabriel C. Carrero, Eduardo de A.S. Florence, Edenise Garcia, Eduardo Trevisan Gonçalves,
Casio Trajano da Luz, Giovanni M. Mallman, Bernardo B.N. Strassburg, Judson F. Valentim
and Agnieszka Latawiec
Results from On-The-Ground Efforts to Promote Sustainable Cattle Ranching in the Brazilian
Amazon
Reprinted from: Sustainability 2018, 10, 1301, doi:10.3390/su10041301 . . . . . . . . . . . . . . . . 65

Ana Beatriz Santos and Marcos Heil Costa

Do Large Slaughterhouses Promote Sustainable Intensification of Cattle Ranching in Amazonia
and the Cerrado?
Reprinted from: Sustainability 2018, 10, 3266, doi:10.3390/su10093266 . . . . . . . . . . . . . . . . 91

Marı́a I. Nieto, Olivia Barrantes, Liliana Privitello and Ramón Reiné

Greenhouse Gas Emissions from Beef Grazing Systems in Semi-Arid Rangelands of Central
Argentina
Reprinted from: Sustainability 2018, 10, 4228, doi:10.3390/su10114228 . . . . . . . . . . . . . . . . 119

Gwendolyn Rudolph, Stefan Hörtenhuber, Davide Bochicchio, Gillian Butler,

Roland Brandhofer, Sabine Dippel, Jean Yves Dourmad, Sandra Edwards, Barbara Früh,
Matthias Meier, Armelle Prunier, Christoph Winckler, Werner Zollitsch and Christine Leeb
Effect of Three Husbandry Systems on Environmental Impact of Organic Pigs
Reprinted from: Sustainability 2018, 10, 3796, doi:10.3390/su10103796 . . . . . . . . . . . . . . . . 141

v
Ilkka Leinonen, Michael MacLeod and Julian Bell
Effects of Alternative Uses of Distillery By-Products on the Greenhouse Gas Emissions of
Scottish Malt Whisky Production: A System Expansion Approach
Reprinted from: Sustainability 2018, 10, 1473, doi:10.3390/su10051473 . . . . . . . . . . . . . . . . 161

Cristina Ullrich, Marion Langeheine, Ralph Brehm, Venja Taube, Diana Siebert and
Christian Visscher
Influence of Reduced Protein Content in Complete Diets with a Consistent Arginine–Lysine
Ratio on Performance and Nitrogen Excretion in Broilers
Reprinted from: Sustainability 2018, 10, 3827, doi:10.3390/su10113827 . . . . . . . . . . . . . . . . 179

Henrik Saxe, Lorie Hamelin, Torben Hinrichsen and Henrik Wenzel

Production of Pig Feed under Future Atmospheric CO2 Concentrations: Changes in Crop
Content and Chemical Composition, Land Use, Environmental Impact, and Socio-Economic
Consequences
Reprinted from: Sustainability 2018, 10, 3184, doi:10.3390/su10093184 . . . . . . . . . . . . . . . . 192

Katrin Gerlach, Alexander J. Schmithausen, Ansgar C. H. Sommer, Manfred Trimborn,

Wolfgang Büscher and Karl-Heinz Südekum
Cattle Diets Strongly Affect Nitrous Oxide in the Rumen
Reprinted from: Sustainability 2018, 10, 3679, doi:10.3390/su10103679 . . . . . . . . . . . . . . . . 210

Michael MacLeod, Vera Eory, William Wint, Alexandra Shaw, Pierre J. Gerber,
Giuliano Cecchi, Raffaele Mattioli, Alasdair Sykes and Timothy Robinson
Assessing the Greenhouse Gas Mitigation Effect of Removing Bovine Trypanosomiasis in
Eastern Africa
Reprinted from: Sustainability 2018, 10, 1633, doi:10.3390/su10051633 . . . . . . . . . . . . . . . . 223

Ricarda Maria Schmithausen, Sophia Veronika Schulze-Geisthoevel, Céline Heinemann,

Gabriele Bierbaum, Martin Exner, Brigitte Petersen and Julia Steinhoff-Wagner
Reservoirs and Transmission Pathways of Resistant Indicator Bacteria in the Biotope Pig Stable
and along the Food Chain: A Review from a One Health Perspective
Reprinted from: Sustainability 2018, 10, 3967, doi:10.3390/su10113967 . . . . . . . . . . . . . . . . 238

Marco Baldi, Maria Cristina Collivignarelli, Alessandro Abbà and Ilaria Benigna
The Valorization of Ammonia in Manure Digestate by Means of Alternative Stripping Reactors
Reprinted from: Sustainability 2018, 10, 3073, doi:10.3390/su10093073 . . . . . . . . . . . . . . . . 264

vi
About the Special Issue Editor
Ilkka Leinonen (Dr) works at the Department of Rural Economy, Environment and Society at
Scotland’s Rural College (SRUC), United Kingdom. He obtained his PhD from the University of
Joensuu (Finland) in 1997 and has since then carried out agricultural, ecological, and environmental
research, with a main interest in quantitative methodologies, especially process-based modelling
of ecosystem carbon, water, and nutrient dynamics. During recent years, he has mainly
focused on the environmental sustainability of agricultural production systems, using and further
developing methods of life cycle assessment (LCA) to quantify greenhouse gas emissions and other
environmental impacts of agriculture and to investigate mitigation strategies in the livestock sector,
for example, through changes in feeding, breeding, housing, and manure management. His other
expertise includes ecophysiological plant and animal modelling, physical energy balance modelling,
and methods for image analysis and remote sensing.

vii
Preface to ”Environmentally Sustainable Livestock
Production”
Livestock production is a major global source of greenhouse gas emissions and it is also
associated with other environmental issues, such as ammonia emissions and regional nutrient
imbalances. This Special Issue presents 14 scientific papers assessing measures that aim to improve
the environmental sustainability of livestock production and to mitigate its environmental impacts.
Globally, the most important livestock species (beef and dairy cattle, pigs, broiler chicken and
laying hens) are covered in the papers. The scope of the papers ranges from farm level mitigation
methods to national level system changes. In general, most of the papers identify the efficiency of
production as a key factor affecting the emissions arising from the livestock sector. In many studies,
holistic approaches, such as environmental life cycle assessment, are used to assess the possible
improvements in emission intensity, and the required links to other dimensions of sustainability,
for example, using the methodology of social life cycle assessment, are also demonstrated in this
Special Issue.

Ilkka Leinonen
Special Issue Editor

ix
 sustainability

Editorial
Achieving Environmentally Sustainable
Livestock Production
Ilkka Leinonen
Department of Rural Economy, Environment and Society, Scotland’s Rural College (SRUC), Peter Wilson
Building, Kings Buildings, West Mains Road, Edinburgh EH9 3JG, UK; [email protected];
Tel.: +44-131-5354044

Received: 2 January 2019; Accepted: 4 January 2019; Published: 7 January 2019

Livestock production is a major global source of greenhouse gas emissions [1] and high density of
livestock in certain areas can also create local environmental issues such as harmful levels of ammonia
emissions and regional nutrient imbalances [2,3]. However, future improvements in the global livestock
sector can also be seen as a potential opportunity for delivering a significant share of the necessary
mitigation of global warming and other environmental problems [1]. In fact, it has been demonstrated
that significant reductions in various environmental impacts and especially in the emissions intensities
(i.e., the amount of emissions per unit of product) have been already achieved in livestock production
during the past decades, for example through breeding, optimized feeding, improved health status of
animals, and improved manure management [4–6].
This Special Issue presents results from studies on different measures aiming to improve the
environmental sustainability of livestock production and to mitigate environmental impacts, including
emissions of greenhouse gases (carbon dioxide, methane, and nitrous oxide), nitrogen and phosphorus
excretion, ammonia emissions, land use and use of energy and other resources. Globally the most
important livestock species (beef and dairy cattle, pigs, broiler chicken and laying hens) are covered
in the papers published here. The mitigation methods assessed in the papers include general system
changes (together with novel approaches to comparison of alternative production systems), changes in
feeding, improvement of animal health, and new technologies of manure management.
The scope of the papers included in this Special Issue range from farm level mitigation methods to
national level system changes. One of the national-level articles, written by Pelletier et al. [7], presents
an overview of the sustainability of the Canadian egg production industry. The authors provide
an interdisciplinary perspective to this industry, considering its past, present, and potential futures.
Their analysis covers environmental, institutional, and socio-economic sustainability with a special
emphasis on animal welfare. The analysis identifies major challenges for sustainable egg industry,
including shifting consumer and other stakeholder preferences and expectations, and conflicts between
the expectations and scientific evidence. A thorough discussion is provided on possible strategies to
resolve these issues.
The methodology of Life Cycle Assessment (LCA) is becoming a standard in evaluating the
environmental sustainability of livestock systems, but LCA also has applications in the areas of
social (S-LCA) and economic (life cycle costing) sustainability assessment. In contrast to relatively
well established methods of environmental Life Cycle Assessment, the methods of S-LCA are still
under development. In his second paper in this Special Issue, Nathan Pelletier [8] develops a suite
of context-appropriate indicators and metrics to characterize the social risks and benefits specific
to activities at Canadian egg production facilities and then applies those indicators to perform a
detailed assessment of the “gate-to-gate” social risks and benefits of Canadian egg production facilities.
The analysis presented here provides a starting point for expanding the methodology to cover the
whole production chain and thus enable a full social life cycle assessment.

Sustainability 2019, 11, 246; doi:10.3390/su11010246 1 www.mdpi.com/journal/sustainability

Sustainability 2019, 11, 246

In their paper, Cai et al. [9] carry out a national level study on a reduction of the emission intensities
(per unit of the monetary value of output) of non-CO2 greenhouse gases arising from the livestock
sector in China, through an analysis of the contribution of each province to the overall national
emissions. They especially concentrate on the role of three “driving factors,” i.e., environmental
efficiency, productive efficiency and economic share, in determining the national greenhouse gas
emission intensity. Their findings suggest that the productive efficiency (i.e., the input of production
factors per unit of output value) is the main contributor to the changes in the emission intensities,
and improvement in this factor has resulted in a considerable reduction of livestock sector emission
intensity at the national level during the period of 1997–2016.
The effect of system changes on the productivity of cattle production in the Amazon biome was
evaluated by zu Ermgassen et al. [10]. The key question in their study is how to handle the increasing
agricultural production in Brazil (e.g., currently the World’s second largest cattle herd) and at the same
time protect remaining natural vegetation. The authors found that currently the cattle productivity in
the Amazon biome is very low, and intensification of the cattle production systems would be the key
factor in achieving higher environmental sustainability. In their paper, they present results from six
initiatives in the Brazilian Amazon, which have successfully improved the productivity in beef and
dairy systems.
Brazilian livestock production is also considered in the paper by Santos and Costa [11]. They tested
the hypothesis according to which large slaughterhouses are potential leverage points for promoting
sustainable intensification in the beef supply chain in Amazonia and the Cerrado, due to their
interactions with ranchers, their location at the agricultural frontier, and their ability to control access
to the market. The authors’ conclusion was that although cattle-ranching intensification (with positive
effect on environmental indicators) has occurred in the Cerrado, this development is independent of
the presence of large slaughterhouses. Instead, the authors suggest that conservation measures such as
a strong monitoring systems and more restrictive environmental policies would be the key promotes
of environmental sustainability, especially at the Amazonia region.
In their article, Nieto et al. [12] assess the on-farm greenhouse gas emissions from beef production
in semi-arid rangelands in Argentina and apply statistical analyses to identify the relationship
between emissions and current farm management practices. Their results highlight the importance of
efficient production in achieving environmental sustainability of livestock production. Their findings
indicate that the emissions per product were low on farms that had improved livestock care
management, applied rotational grazing, and had access to technical advice. The authors suggest that
“implementation of realistic, relatively easy-to-adopt farming management practices has considerable
potential for mitigating the GHG emissions in the semi-arid rangelands of central Argentina.”
Livestock production in Europe has been considered to be highly intensive, and thus relatively
efficient. However, many low-intensity systems exist as well, especially in organic production. In the
study by Rudolph et al. [13] a system comparison using environmental LCA was carried for three
European organic pig production systems, namely indoor, partly outdoor, and outdoor. The authors
found a great between-farm variation in three environmental indicators: global warming, acidification
and eutrophication potentials. The differences between the farms were mainly affected by feed
production and to some extent also by housing. There were no between-system differences in global
warming potential, but acidification potential was highest in the indoor system (as a result of ammonia
emissions) and the eutrophication potential highest in the outdoor system (as a result of nutrient
leaching). The authors conclude that the occurrence of organic farms with low environmental impacts
indicates that it is possible to manage organic pig production in an environmentally friendly way.
Using agricultural by-products (that are not suitable for human consumption) as part of livestock
feed has been considered to be one method to improve the environmental sustainability of livestock
production. In their study, Leinonen et al. [14] assess the environmental consequences of using distillery
by-products as a protein source for beef cattle in Scotland. Their study highlights the complexity
of livestock feed production chains. This was demonstrated by the alternative uses of agricultural

2
Sustainability 2019, 11, 246

by-products (in this case either as a livestock feed or as a source of renewable energy), and the
environmental impacts arising from those options were analyzed through the system expansion-based
LCA approach.
Another option to reduce the environmental impacts through livestock feeding is to apply resource
efficient feed formulation. Ullrich et al. [15] evaluated the potential of reducing the crude protein level
of the broiler diet by using supplementation of single amino acids to achieve an optimum amino acid
balance of the feed. Their experimental results confirm some earlier modelling studies [16] according
to which a balanced diet with lowered crude protein concentration can reduce the amount of nitrogen
excreted, which has multiple environmental benefits. It is also demonstrated that such an improvement
can be achieved without compromising animal performance.
The link between livestock feeding and climate change is not only a one direction process. The feed
formulation in the future may also be affected by changes in the availability and quality of certain
feed ingredients, and such changes can be induced by global warming and increased atmospheric
CO2 concentration. Saxe et al. [17] applied a consequential life cycle assessment to quantify the
environmental impacts and socio-economic effects that altered crop yields and chemical composition
of the crops at elevated CO2 levels in the future can have on pig feed formulation. They predict that
the elevated CO2 reduces the land use demand for pig feed production, but at the same time increases
the demand for protein crops (soya), due to reduced protein concentration of feed crops. This will
have considerable environmental and economic consequences.
In cattle production, methane from enteric fermentation and manure management is generally
considered to be the most significant greenhouse gas. However, nitrous oxide emissions related to
ruminant feeding have also their own role in the total emissions from this livestock sector. In their
article, Gerlach et al. [18] present a new method for determining the concentrations of CO2 , CH4 , and
N2 O in the ruminal gas phase of steers after ingestion of different forage types. Depending on the diet,
high concentration of N2 O were found in the rumen, indicating that that fermented forages rich in
nitrogen can be a significant source of greenhouse gases.
Improving the health status of animals is one option to maintain high production efficiency
of livestock and in this way keep the emission intensity at the minimal level. In their paper,
MacLeod et al. [19] apply the FAO livestock model GLEAM to quantify the greenhouse gas emissions
from East African cattle production systems and the effects of an endemic disease trypanosomiasis on
the emissions. The authors found that removing that disease could lead to a reduction in the emissions
intensity per unit of protein produced, as a result of increases in milk yields and higher cow fertility
rates. Another major issue related to animal health is antibiotic resistance, and this has also links to the
environmental impacts of livestock production. In their comprehensive review, Schmithausen et al. [20]
highlight knowledge gaps and various factors that contribute to the transmission of antibiotic-resistant
bacteria between animals, humans, and the environment in pig production, following a holistic “One
Health” approach.
Although most papers in this special issue focus on livestock husbandry and its effect on animal
performance when considering possible methods for reducing the environmental impacts of livestock
system (and their potential effects on human health), different manure management options can
potentially also control such impacts. Reduction of ammonia emission through improved manure
management has direct consequences on human and animal health, and it also affects numerous
environmental issues such as eutrophication, acidification, and global warming. In this Special Issue,
novel technologies of manure management are considered in the paper by Baldi et al. [21], who show
results of a comparison of ammonia stripping methods aiming to reduce the emissions arising from
digestate derived from anaerobic digestion of livestock manure and corn silage.
In summary, this Special Issue demonstrates a range of opportunities that would help to reduce
the environmental impacts of global livestock production. Most of the papers identify the efficiency
of the production as a key factor to affect the emission intensity of the livestock products. To assess
the possible improvements in efficiency, holistic approaches such as Live Cycle Assessment would

3
Sustainability 2019, 11, 246

be necessarily needed, and further methodological development in this area is still required [22].
This would be especially a challenge when linking together the three pillars of sustainability
(environmental, social, and economic) in sustainability assessments of livestock production.

Funding: This research was partly funded by the Scottish Government Rural Affairs and the Environment
Portfolio Strategic Research Programme 2016-2021, WP 1.4 ‘Integrated and Sustainable Management of Natural
Assets’ and 2.4 ‘Rural Industries’.
Conflicts of Interest: The author declares no conflict of interest.

References
1. Gerber, P.J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling
Climate Change through Livestock. A Global Assessment of Emissions and Mitigation Opportunities; Food and
Agriculture Organization of the United Nations (FAO): Rome, Italy, 2013; ISBN 978-92-5-107921-8.
2. Vitousek, P.M.; Naylor, R.; Crews, T.; David, M.B.; Drinkwater, L.E.; Holland, E.; Johnes, P.J.; Katzenberger, J.;
Martinelli, L.A.; Matson, P.A.; et al. Nutrient imbalances in agricultural development. Science 2009, 324,
1519–1520. [CrossRef]
3. Leinonen, I.; Eory, V.; MacLeod, M. Applying a process-based livestock model to predict spatial variation in
agricultural nutrient flows in Scotland. J. Clean. Prod. 2018, 209, 180–189. [CrossRef]
4. Pelletier, N.; Ibarburu, M.; Xin, H. Comparison of the environmental footprint of the egg industry in the
United States in 1960 and 2010. Poult. Sci. 2014, 93, 241–255. [CrossRef] [PubMed]
5. Tallentire, C.W.; Leinonen, I.; Kyriazakis, I. Breeding for efficiency in the broiler chicken. A review.
Agron. Sustain. Dev. 2016, 36, 66. [CrossRef]
6. Tallentire, C.W.; Leinonen, I.; Kyriazakis, I. Artificial selection for improved energy efficiency is reaching its
limits in broiler chickens. Sci. Rep. 2018, 8, 116. [CrossRef] [PubMed]
7. Pelletier, N.; Doyon, M.; Muirhead, B.; Widowski, T.; Nurse-Gupta, J.; Hunniford, M. Sustainability in
the Canadian Egg Industry—Learning from the Past, Navigating the Present, Planning for the Future.
Sustainability 2018, 10, 3524. [CrossRef]
8. Pelletier, N. Social Sustainability Assessment of Canadian Egg Production Facilities: Methods, Analysis, and
Recommendations. Sustainability 2018, 10, 1601. [CrossRef]
9. Cai, T.; Yang, D.; Zhang, X.; Xia, F.; Wu, R. Study on the Vertical Linkage of Greenhouse Gas Emission
Intensity Change of the Animal Husbandry Sector between China and Its Provinces. Sustainability 2018, 10,
2492. [CrossRef]
10. Zu Ermgassen, E.; Alcântara, M.; Balmford, A.; Barioni, L.; Neto, F.; Bettarello, M.; Brito, G.; Carrero, G.;
Florence, E.; Garcia, E.; et al. Results from On-The-Ground Efforts to Promote Sustainable Cattle Ranching in
the Brazilian Amazon. Sustainability 2018, 10, 1301. [CrossRef]
11. Santos, A.; Costa, M. Do Large Slaughterhouses Promote Sustainable Intensification of Cattle Ranching in
Amazonia and the Cerrado? Sustainability 2018, 10, 3266. [CrossRef]
12. Nieto, M.; Barrantes, O.; Privitello, L.; Reiné, R. Greenhouse Gas Emissions from Beef Grazing Systems in
Semi-Arid Rangelands of Central Argentina. Sustainability 2018, 10, 4228. [CrossRef]
13. Rudolph, G.; Hörtenhuber, S.; Bochicchio, D.; Butler, G.; Brandhofer, R.; Dippel, S.; Dourmad, J.; Edwards, S.;
Früh, B.; Meier, M.; et al. Effect of Three Husbandry Systems on Environmental Impact of Organic Pigs.
Sustainability 2018, 10, 3796. [CrossRef]
14. Leinonen, I.; MacLeod, M.; Bell, J. Effects of Alternative Uses of Distillery By-Products on the Greenhouse
Gas Emissions of Scottish Malt Whisky Production: A System Expansion Approach. Sustainability 2018, 10,
1473. [CrossRef]
15. Ullrich, C.; Langeheine, M.; Brehm, R.; Taube, V.; Siebert, D.; Visscher, C. Influence of Reduced Protein
Content in Complete Diets with a Consistent Arginine–Lysine Ratio on Performance and Nitrogen Excretion
in Broilers. Sustainability 2018, 10, 3827. [CrossRef]
16. Leinonen, I.; Williams, A.G. Effects of dietary protease on nitrogen emissions from broiler production: A
holistic comparison using Life Cycle Assessment. J. Sci. Food Agric. 2015, 95, 3041–3046. [CrossRef]

4
Sustainability 2019, 11, 246

17. Saxe, H.; Hamelin, L.; Hinrichsen, T.; Wenzel, H. Production of Pig Feed under Future Atmospheric CO2
Concentrations: Changes in Crop Content and Chemical Composition, Land Use, Environmental Impact,
and Socio-Economic Consequences. Sustainability 2018, 10, 3184. [CrossRef]
18. Gerlach, K.; Schmithausen, A.; Sommer, A.; Trimborn, M.; Büscher, W.; Südekum, K. Cattle Diets Strongly
Affect Nitrous Oxide in the Rumen. Sustainability 2018, 10, 3679. [CrossRef]
19. MacLeod, M.; Eory, V.; Wint, W.; Shaw, A.; Gerber, P.; Cecchi, G.; Mattioli, R.; Sykes, A.; Robinson, T.
Assessing the Greenhouse Gas Mitigation Effect of Removing Bovine Trypanosomiasis in Eastern Africa.
Sustainability 2018, 10, 1633. [CrossRef]
20. Schmithausen, R.; Schulze-Geisthoevel, S.; Heinemann, C.; Bierbaum, G.; Exner, M.; Petersen, B.;
Steinhoff-Wagner, J. Reservoirs and Transmission Pathways of Resistant Indicator Bacteria in the Biotope Pig
Stable and along the Food Chain: A Review from a One Health Perspective. Sustainability 2018, 10, 3967.
[CrossRef]
21. Baldi, M.; Collivignarelli, M.; Abbà, A.; Benigna, I. The Valorization of Ammonia in Manure Digestate by
Means of Alternative Stripping Reactors. Sustainability 2018, 10, 3073. [CrossRef]
22. Mackenzie, S.G.; Leinonen, I.; Kyriazakis, I. The need for co-product allocation in the Life Cycle Assessment
of agricultural systems—Is “biophysical” allocation progress? Int. J. Life Cycle Assess. 2017, 22, 128–137.
[CrossRef]

© 2019 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

5
 sustainability

Article
Sustainability in the Canadian Egg
Industry—Learning from the Past,
Navigating the Present, Planning for the Future
Nathan Pelletier 1, * , Maurice Doyon 2 , Bruce Muirhead 3 , Tina Widowski 4 ,
Jodey Nurse-Gupta 5 and Michelle Hunniford 6
1 340 Charles Fipke Centre for Innovative Research, 3247 University Way, University of British Columbia,
Kelowna, BC V1V1V7, Canada
2 Department of Agricultural Economics and Consumer Science, Laval University, Quebec City, QC G1V 0A6,
Canada; [email protected]
3 Research Oversight and Analysis and Department of History, University of Waterloo, Waterloo,
ON N2L 3G1, Canada; [email protected]
4 Department of Animal Biosciences, University of Guelph, Guelph, ON N1G2W1, Canada;
[email protected]
5 Department of History, University of Waterloo, Waterloo, ON N2L 3G1, Canada; [email protected]
6 Burnbrae Farms Ltd., Lyn, ON K0E1M0, Canada; [email protected]
* Correspondence: [email protected]; Tel.: +1-250-807-8245

Received: 30 August 2018; Accepted: 27 September 2018; Published: 30 September 2018

Abstract: Like other livestock sectors, the Canadian egg industry has evolved substantially over
time and will likely experience similarly significant change looking forward, with many of these
changes determining the sustainability implications of and for the industry. Influencing factors
include: technological and management changes at farm level and along the value chain resulting
in greater production efficiencies and improved life cycle resource efficiency and environmental
performance; a changing policy/regulatory environment; and shifts in societal expectations and
associated market dynamics, including increased attention to animal welfare outcomes—especially
in regard to changes in housing systems for laying hens. In the face of this change, effective
decision-making is needed to ensure the sustainability of the Canadian egg industry. Attention
both to lessons from the past and to the emerging challenges that will shape its future is required
and multi- and interdisciplinary perspectives are needed to understand synergies and potential
trade-offs between alternative courses of action across multiple aspects of sustainability. Here, we
consider the past, present and potential futures for this industry through the lenses of environmental,
institutional (i.e., regulatory), and socio-economic sustainability, with an emphasis on animal welfare
as an important emergent social consideration. Our analysis identifies preferred pathways, potential
pitfalls, and outstanding cross-disciplinary research questions.

Keywords: Canada; eggs; sustainability; animal welfare; economics; supply management

1. Introduction
Food systems are at the center of human well-being. In addition to satisfying a basic human need
(i.e., regular access to food in sufficient quantity and of sufficient quality), food is also often a central
contributor to our economies and cultures, and often even to our individual identities. However,
activities in the agri-food system are also at the center of many of our most pressing sustainability
challenges. The production of food—in particular, in the livestock sector—contributes a large fraction of
current anthropogenic resource demands and environmental pressures [1–3]. For this reason, livestock
industries are naturally the focus of a growing body of sustainability research and management
initiatives [4].

Sustainability 2018, 10, 3524; doi:10.3390/su10103524 6 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3524

Taken together with projected increases in food production globally and a trend towards diets
higher in livestock products, this has spurred considerable interest in the concept and practice of
“sustainable intensification” in the livestock sector [4]. According to Pretty et al. [5], sustainable
intensification is defined as “producing more output from the same area of land while reducing
negative environmental impacts and at the same time increasing contributions to natural capital and
the flow of environmental services.” Clearly, however, sustainable intensification efforts may also have
potential benefits and trade-offs across socio-economic, institutional, and other aspects of sustainability
that must be carefully considered.
Life cycle thinking (LCT) has emerged as a core concept in sustainability science [6]. LCT refers to
adopting a systems-level perspective on industrial activities. This perspective enables us to understand
how different kinds of potential sustainability benefits and impacts are distributed along agri-food
supply chains, as well as trade-offs that may occur with respect to different valued outcomes when
particular changes are implemented. Environmental life cycle assessment (e-LCA) is a commonly
used tool, based on LCT, for studying and managing the resource/environmental dimensions of food
supply chains [4]. In recent years, a rich body of research has applied this tool to evaluate a variety of
livestock production systems and technologies in different contexts, and as a basis for understanding
the respective merits of potential sustainable intensification technologies (for a review of 173 recent
papers, see McClelland et al. [7]).
While such research is clearly of considerable value, it is by itself insufficient to support
sustainability decision-making for the livestock sector since it considers only a subset of important
sustainability criteria that inform our decisions [8]. In reality, the varied forces that influence how we
produce and consume livestock products along with the associated benefits and impacts are complex,
often interacting, and variable over time. They include changes in technology and management
practices, evolving societal expectations and consumer preferences, and the regulatory context in
which specific industries operate. Efforts to understand current sustainability challenges in the
livestock sector and to identify preferred paths forward can benefit from interdisciplinary approaches
that evaluate these forces with respect to historical trends, current conditions, and possible futures.
Egg Farmers of Canada, the industry body governing the production and marketing of eggs within
the supply-managed Canadian egg industry, provides research monies to support four Research Chairs
at Canadian universities. These Research Chairs respectively undertake independent research in the
fields of economics (Doyon), public policy (Muirhead), animal welfare (Widowski), and sustainability
(Pelletier) of broad or direct relevance to the egg industry. The current analysis brings together the
expertise, research, and perspectives of each of these Chairs to present an integrated study of the
past, present and possible futures for this industry. Specifically, the purpose of the analysis is to
identify: (1) the key factors that have shaped the modern Canadian egg industry; (2) the issues
and opportunities it currently faces; and (3) potential synergies and trade-offs across the multiple
dimensions of sustainability that should be considered on an interdisciplinary basis in choosing among
viable paths looking forward.

2. Methods
The analysis is presented in three sections. The first section provides a historical perspective,
describing the emergence and evolution of the Canadian egg industry over the past century until the
present. It is organized into subsections respectively addressing: key technological and management
changes, including their influence on the efficiency and environmental sustainability impacts of
egg production; the development and implications of the supply management system that governs
the industry; the factors that have influenced the economics of egg production, including changing
consumer preferences and social expectations; and, as an important aspect of the latter, the emergence
of animal welfare as both a societal concern and field of study/application for the egg industry.
The second section, also organized into four subsections, describes challenges that the industry
currently faces in each of these domains that may undermine its sustainability, as well as potential

7
Sustainability 2018, 10, 3524

solutions. Possible trade-offs across sustainability domains that such solutions may imply are identified.
On this basis, the final section summarizes some of the key areas for interdisciplinary research and
collaboration that are necessary to support choosing among alternative courses of action to enable a
sustainable egg industry in Canada into the future.

3. Discussion

3.1. Canadian Egg Industry Retrospective (Circa 1920 to Present)

3.1.1. Technology, Management, and Resource Efficiency

Although a small number of specialized, commercial egg farms in Canada existed in the early
part of the 20th century, egg production was generally one among a series of activities undertaken on
the mixed-farming operations that were characteristic of Canadian agriculture at that time. Beginning
in the 1920s, however, the egg industry entered a period of significant and sustained industrialization.
Two major developments that were particularly important to the specialization and intensification
of egg production were the adoption of cage systems for housing laying hens and improved genetic
selection for egg production and feed conversion efficiency.
From 1923–1924, D.C. Kennard performed the first experiments keeping laying hens in
confinement at the Ohio Agricultural Research Station, using livability and production as the main
measures of success [9]. However, cage systems were not immediately adopted for commercial use.
This was because indoor confinement for longer periods of time was only possible once the complete
ration, which was developed in 1924, was made available on the wider market in 1929 and the Rural
Electrification Act of 1936 in the US enabled barns to be lit artificially. The ability to keep laying hens
indoors revolutionized the egg industry [10,11]. Whereas eggs were previously a seasonal (spring)
food in temperate climates, they could now be produced continuously year-round [12].
According to Lee, 1938 marked the year when farmers had “satisfactorily solved the many
problems of management which were responsible for the failure of earlier battery plants (so called
because of the methodical (militaristic) nature of organizing the cages in stacked groups or
batteries)” [10]. The need for steel during World War II, however, meant that the production of
cages was halted (except for a small number of chick batteries) until after the war when the battery
cage boom started on the Pacific coast of the US and in the UK [10].
Individual cages were initially used because they eliminated issues with cannibalism and allowed
for the practice of “positive culling,” or removing birds from the flock that are “laying at a slow
unprofitable rate or [have] quit laying altogether” [13]. However, due to the cost advantages of
housing multiple birds in the same cage, the battery cage was adapted to house small groups of
hens [14]. Beginning in the 1960s egg production in Canada transitioned from “free-run” (i.e., indoor
non-cage) to cage-based production.
Genetic selection of laying hens for egg production and feed use efficiency in cage systems also
began in earnest following World War II. Canadian Donald Shaver built a global breeding organization
for layer and broiler strains [15]. The availability of electricity-powered incubators and the relatively
short incubation cycle for eggs facilitated rapid progress in selection for production efficiency [16].
At the same time, development of improved management practices for disease prevention such as
biosecurity protocols, along with the advent of poultry vaccines, served to improve bird health and
reduce losses due to mortality [17,18]. Over time, advancements in housing technology including
artificial ventilation systems and climate control, automated feeding, egg collection and manure
removal were implemented, thereby reducing labor and allowing for thousands or tens of thousands
of birds to be housed in a single barn.
In combination, these technology and management changes have enabled considerable
improvements in resource efficiency and the reduction of environmental impacts associated with
producing eggs in Canada. For example, annual rate of lay among Canadian laying hens has increased
from less than 100 eggs per year in the early 20th century to over 300 at present [19]. Between 1962

8
Sustainability 2018, 10, 3524

and 2012, an interval of 50 years, rate of lay increased by more than 50%. This same 50-year interval
was also marked by declining mortality rates (falling from roughly 13% in the early 1960s to 3.2% at
present for pullets and laying hens combined), and by much improved feed conversion efficiencies.
With respect to the latter, producing 1 kg of eggs in 1962 required over 3 kg of feed compared to the
current average of 2 kg on contemporary egg farms [20].
Efficiency changes have been equally pronounced along the supply chains that ultimately
support Canadian egg production. Among these, the most influential in terms of life cycle resource
use/emissions-related sustainability impacts have been: (a) a 50% reduction in the energy intensity of
ammonia production for nitrogen fertilizers (one of the most energy and emissions intensive aspects
of modern agriculture); (b) improved yield-to-fertilizer and energy input ratios for the production of
agricultural feed inputs (for example, corn yields in the province of Ontario increased 96% over this
interval while nitrogen inputs per ton of crop declined 44%); and (c) improved efficiencies in freight
transport, which connect activities all along the Canadian egg supply chain [20].
As a result, of these changes, the overall environmental footprint (i.e., including all supply chain
activities) of producing eggs in Canada has, on average, declined 61%, 68%, and 72% for acidifying,
eutrophying, and greenhouse gas (GHG) emissions while energy, land and water use decreased
by 41%, 81% and 69% respectively per unit production. Moreover, despite that egg production
volumes roughly doubled in Canada since the early 1960s, the absolute resource and environmental
impacts for the industry as a whole were estimated to be 41%, 51% and 57% lower for acidifying,
eutrophying, and greenhouse gas emissions, respectively. Supply chain energy, land and water use
are 10%, 71% and 53% lower in aggregate [20]. These changes reflect a combination of farm-level
efficiency gains (15–40%, depending on impact category) associated with improved management
practices, superior bird genetics, and vaccine developments; changes in feed composition (29–60%);
and changing efficiencies in activities along the supply chains that ultimately support egg production
(0–56%) [20].
Life cycle assessment research has hence enabled a nuanced understanding of both the magnitude
and distribution of a variety of environmental sustainability impacts along the contemporary Canadian
egg supply chain, the relative importance of specific inputs to and activities associated with egg
production as sources of these impacts, and the comparative impacts of egg production in alternative
housing systems [21]. A relatively small number of variables explain the characteristic sources and
distribution of life cycle resource use and emissions for eggs and egg product supply chains in Canada.
Among these, feed composition and feed conversion efficiency in pullet and (in particular) layer
facilities emerge as the strongest explanatory variables. Manure management is the second critical
determinant of life cycle resource efficiency and emissions. Manure-related emissions are influenced
by several factors, including feed composition (i.e., N and P content of feed inputs), feed conversion
efficiencies, and manure handling strategies. Although more strongly influenced by supply chain
feed inputs, direct water and energy use in facilities also make non-trivial contributions to the overall
water and energy resource requirements for egg production. The contributions of egg processing and
packaging, as well as egg breaking and further processing to overall supply chain resource use and
emissions for eggs and egg products are relatively small [21]. These insights are largely consistent with
similar research of intensive egg production in other countries (for example, [18,22–27]).
Pelletier [21] reported resource efficiencies and life cycle environmental performance by housing
system type for the Canadian egg industry in 2012. Among the five housing technologies considered
(i.e., conventional cages, enriched colony cages (which provide all of the equipment found in
conventional cages with the addition of equipment that is intended to allow hens to express some of
their behavioral priorities), free-run, free-range, and organic), both the life cycle inventory and impact
assessment results suggested fairly similar levels of performance between systems for most variables.
Feed conversion efficiencies were slightly higher in cage-based production, and mortality rates were
substantially lower compared to non-cage systems. Of note was the higher variability in performance
levels observed between reporting facilities for non-cage production systems, likely reflecting the

9
Sustainability 2018, 10, 3524

substantial research and development investments and management experience gained for cage-based
production over time relative to the emerging cage-free sector. Only for organic production were life
cycle resource use and emissions significantly different from the other housing systems [21]. Here,
the lower observed resource use and emissions intensity of organic eggs was attributable to the
lower impacts of feed production rather than differences in farm-level efficiencies, where mortality
rates were highest among the housing systems considered. At present, over 80% of laying hens in
Canada are kept in conventional cages, and the remainder in either enriched cages, free-run barns, or
free-range systems.

3.1.2. Shifting Regulatory Conditions for the Production and Marketing of Eggs
The intensification of the egg industry from the 1920s onward meant that increasing numbers of
eggs were finding their way onto the market. While the consumption of eggs rose steadily over time,
the growth in egg production often outstripped demand, leading to overproduction and hardship for
egg farmers [28,29]. Critically, farmers only received prices that allowed a fair return for short periods
of time after low prices had pushed out the most vulnerable producers. While a shortage of product
briefly forced prices up, the cycle would start over as farmers re-entered the business or ramped up
production and again prices would plummet due to an oversupply of eggs. This was a perennial
problem and the Canadian Minister of Agriculture in 1959, Douglas Harkness, noted that “The only
long-term solution to the current problem is a decrease in egg production to the point where there is a
more realistic balance between supply and domestic requirements” [30].
An additional complication was cheap egg imports from the United States. This meant Canadian
farmers often had to accept egg prices that not only reflected tough domestic competition, but also
a cheaper international price. The US, with its more robust economies of scale, undercut Canadian
prices. Furthermore, provinces with surplus production would seek markets outside their borders,
often undercutting prices and causing local producers’ incomes to drop [31].
The new realities of the price-cost squeeze borne by agricultural producers and trends towards
more specialized, capitalized, and vertically integrated operations caused significant concern among
family farmers who saw producer prices drop and their earnings decrease despite ever more costly farm
investments. While some industry experts believed that the movement towards vertical integration
was inevitable and that only a few of the largest Canadian egg producers would survive, others
argued that egg producers needed to create a system that would permit them to succeed without the
corporatization of the family farm [32,33].
The continued instability of egg prices galvanized discussions about the need for farmers to
organize and institute measures that would secure fair returns. Foremost among these discussions
were proposals to create provincial marketing boards to regulate the production and sale of eggs on a
quota system basis. Critics of the idea of marketing boards cited infringements on their freedom to act
independently. Some egg farmers also recognized that provincial production quotas would only work
if a national production plan were instituted that addressed the issue of egg imports from the US [34].
In July 1971, provincial representatives reached an agreement in principle whereby production
would be controlled by marketing boards in each province and the national market would be shared
based on average production figures calculated from 1968 to 1970. This led to the passage of the Farm
Products Marketing Agencies Act in January 1972, which allowed for the creation of the Canadian
Egg Marketing Agency (CEMA) later that year. The system of “supply management” had come to the
Canadian egg industry [35].
Despite some initial growing pains, by 1976 CEMA had turned the corner, becoming solvent and
revising and consolidating the comprehensive egg marketing plan, which meant uniform pricing,
quota planning, and overproduction penalties introduced in all provinces. The processes were coming
into place that allowed for the successful operation of a national supply management system that
promoted its social and economic sustainability. The system of supply management helped end market
chaos and enabled farmers to earn a living wage and offer consumers a fair price, while demonstrating

10
Sustainability 2018, 10, 3524

a commitment to improved egg farming practices. At present, CEMA, renamed Egg Farmers of Canada
in 2008, oversees the quota-based production and marketing of eggs from over 1000 farms distributed
across all ten Canadian provinces and one territory.

3.1.3. Shifting Social Preferences and Socio-Economic Conditions

Supply Management
Over the years, the economics of the egg industry has been driven by improvements in technology,
genetics, feeds, and management; resulting in productivity gains in rate of lay, in feed conversion and
in lower mortality rates. Supply management, which shaped the marketing of eggs in Canada since
1971, has been similarly important for the economics of egg production, largely through the prevention
of egg surpluses—a primary rationale for its implementation. Production controls were intended to
prevent the boom/bust cycle of commodities production. Whereas the huge swings so characteristic
of commodity sales played havoc with planning and investment [36], supply management provided
income stability for farmers and, for consumers, predictability in meal costing and planning [37].
Price fluctuations were also perceived to favor processors and supermarkets, who drove down
the prices paid to farmers. Indeed, many farmers believed that they were being exploited by several
ruthless buyers who were only interested in making money [38]. In July 1971, for example, a dozen
eggs cost 17 cents retail in Toronto, while the cost of production was about 31 cents. Prices were,
in the words of a Canadian Egg Producers Council document provided to the minister of agriculture,
“disastrously low . . . extending from 1970, through 1971 and the first half of 1972” [39].
As the document went on to note, “Not only this but the public interest is badly served by the
economic waste and inefficiency that is an inevitable consequence of severe cyclical instability, and
by the instability of consumer prices—sometimes extremely (and to the producer disastrously) low,
but at others unnecessarily high as production inevitably falls to inadequate levels under the pressure
of persistent losses.” With the passage of Bill C-176, the Farm Products Marketing Agencies Act on 31
December 1971, the way was clear to establish a national system of egg production, based on provincial
organization, that soon stabilized production, farmer incomes, and consumer prices. Significant
improvement in farm income for egg farmers subsequently allowed them to invest in technology, as
well as to respond to changes in consumer demand, such as for specialty eggs [40].
Although egg farmers’ financial situation has been improved by supply management, eggs in
Canada remain a cheap source of good quality protein. Figure 1 shows that evolution of the index price
for eggs is similar to that of beef, relative to general inflation (CPI). One should note, however, that the
real price (versus the index) of eggs is much cheaper than the price of beef, on a gram of protein basis.

Figure 1. Consumer price index (CPI) for eggs, meat and general inflation in Canada from 1980-2016
(source: Agriculture and Agri-Food Canada [41]).

11
Sustainability 2018, 10, 3524

Shifting Consumer Preferences

The third major variable impacting the economics of egg production has been shifting consumer
preferences. For instance, in 1980, Canadians were consuming roughly 22 dozen eggs a year. However,
due to cholesterol concerns in the 80s and 90s, per capita consumption reached a low of 14.5 dozen in
1995, as illustrated in Figure 2. New research and a better comprehension of the various types of fats
has rehabilitated egg consumption, which has been steadily increasing to the current annual rate of
more than 20 dozen eggs per capita. Thus, Canadian egg farmers have seen steady market growth for
over ten years, after a decade of significant cuts in production quota in the 80s.

Figure 2. Canadian egg consumption (dozen per capita), 1980-2017 (source: Agriculture and Agri-Food
Canada [42]).

Another important change in consumer demand in the 2000’s is seen in the larger share of the
specialty eggs market, which was roughly 12% in Canada in 2017. Specialty eggs are a value-added
product, with differentiation based on either egg composition (omega-3, vitamin D eggs), the perceived
quality (brown eggs), or the conditions under which eggs are produced (organic, free-run, and
free-range eggs), as illustrated in Figure 3.

Figure 3. Specialty eggs in the Canadian market, by attribute.

The emergence of the specialty eggs market reflects the fact that buying food has evolved
from a purely survival focus to include more nuanced nutritional as well as social preferences and
environmental considerations. Animal welfare is an important issue that has been partially addressed
through the offering of specialty eggs with specific animal welfare attributes (Figure 3 under housing).
Those eggs command a higher retail price to reflect higher cost of production [43]. However, a

12
Sustainability 2018, 10, 3524

disconnect between consumer willingness-to-pay and the desire for animal welfare [44] is likely to
result when internalization of animal welfare costs is imposed on producers [45].

3.1.4. Animal Welfare

Public Concern for the Welfare of Laying Hens

Concurrent with the adoption of battery cages came growing public debate regarding the welfare
of laying hens. Newspaper articles as early as 1953 advanced the same arguments that are still
articulated today to either criticize or justify the use of cages. Key criticisms include lack of space,
the inability of hens to perform natural behaviors, and that “the system makes the hen ‘a mere egg
laying machine’” [46]. In defense of cages, arguments are that they decrease disease and facilitate the
provision of clean food and water.
Terms such as laying hen “plants” [10], “factories” or “egg machines” [47] were initially used
to describe production efficiencies and were lauded because of the amount of control given to egg
farmers. In the post-war period, however, such terms were given a negative connotation, and emotive
terminology, for example “concentration camp,” was increasingly used [48]. The book “Animal
Machines” [48], and a subsequent UK government report addressing the welfare of farm animals [14],
criticized animal production systems that severely restrict animal movement and behavior. The
Brambell Report also clarified that a high production rate cannot alone be used as an indicator of good
animal welfare. Nonetheless, by 1970, most hens in Canada (and elsewhere in the developed world)
were kept in battery cages [49].
Beginning in 1976, regulations for animal housing systems in Europe were gradually established,
beginning with the Council of Europe Convention on the Protection of Animals Kept for Farming
Purposes [49]. Over the next few decades, a few individual European countries enacted minimum
space allowances (or outright bans) for hens in cages, and a 1986 EU Directive set a minimum size for
cages. This culminated in the EU Council Directive 99/74 for laying hens, which prohibited the use of
non-enriched cage systems in all EU countries as of January 2012 [50]. According to the Directive, hens
in cages must have a minimum of 750 cm2 per hen and hens in non-cage systems must be stocked no
greater than nine hens per m2 . All hens, regardless of housing system, must have a nest, perches, and
litter to allow pecking and scratching [50]. In 2016, 55.6% of hens in the EU were housed in enriched
cages with the remainder in free-run, free-range, and organic non-cage systems.
In Canada, the process for setting animal welfare standards for farm animals, coordinated by the
Canadian Federation for Humane Societies (CFHS), was initiated in 1980 [51]. This process aimed
to develop voluntary codes of practices for all livestock species. The first Code of Practice for Care
and Handling of Chickens was published in 1983, followed by the Code of Practice for the Care
and Handling of Pullets and Laying hens in 2003. These codes laid out recommendations for space
allowances and other aspects of animal care, primarily for hens housed in battery cages [51]. In 2005,
the National Farm Animal Care Council was established and developed a new and more rigorous
process for developing science-informed codes. Code committees currently include multi-stakeholder
representation from farmers, government agencies, scientists, CFHS, and national food retailer,
restaurant, and food service associations. The process for code development includes establishment of
a scientific committee that drafts a scientific report and review of the literature on key welfare issues,
as well as regular re-evaluation of each code in response to developments in scientific and production
knowledge [51].
In 2012, Egg Farmers of Canada (EFC) initiated a review of the 2003 Code under the guidance of
the National Farm Animal Care Council. The new Code of Practice for laying hens was released in
early 2017. The code requires all hens to be provided nests, perches, scratch mats or foraging material
by 2036, similar to the EU Directive. While allowing for continued adoption of enriched cages, the
code also sets more detailed standards for non-cage systems than are in place in the EU. Although
the codes are not legislated, “when included as part of an assessment program, those who fail to

13
Sustainability 2018, 10, 3524

implement requirements may be compelled by industry associations to undertake corrective measures

or risk a loss of market options. Requirements also may be enforceable under federal and provincial
regulation” [52].

Food Retailers as Drivers of Change

In Canada (and North America more broadly), changes to hen housing based on animal welfare
concerns are coming much later compared to Europe and have been primarily market or producer
driven (in response to pressure from customers and animal protection groups) rather than regulatory.
In 2000, the United Egg Producers (a US trade organization) developed animal husbandry guidelines
and an auditing program that set a minimum space allowance for laying hens in conventional battery
cages [53]. That same year, McDonald’s set a higher minimum space requirement for hens in their egg
supply chain in the USA and Canada [54], followed soon after by Burger King and Wendy’s. Over the
next decade, several US states passed laws that essentially banned conventional cages [53]. However, a
federal bill (The Egg Products Inspection Act Amendment “The Egg Bill)” introduced to US Congress
in 2012 and 2013 that aimed to eliminate conventional battery cages but still allow for the adoption of
enriched cages subsequently failed [55]. Corporate campaigns soon followed to obtain pledges from
major food retailers, food service industries, and food manufacturers to purchase eggs solely from
hens kept in cage-free systems.
In 2015, the first few North American restaurants, grocers and manufacturers made pledges to
purchase eggs only from non-cage systems. In February 2016, EFC announced that no new conventional
cage systems were to be installed after July 2016, but that both enriched cages and non-cage systems
would be allowed. Shortly thereafter, the Retail Council of Canada, which comprises most large grocery
chains in Canada, committed to sourcing only cage-free eggs by the end of 2025 [53]. By the end of
2016, an unprecedented number of North American corporations made commitments to cage-free
housing which will require new or retrofitted barns for over 200 million hens in the United States and
Canada by 2026 [55].

3.2. Canadian Egg Industry Prospective

3.2.1. Current Challenges and Opportunities for Improved Technology, Management, and
Resource Efficiency
Leveraging continued efficiency gains and emissions reductions in the egg industry is important
from the perspective of resource and environmental sustainability and may be supported by four
separate but complementary foci. However, any recommended management or technology initiatives
need necessarily be considered taking into account potential trade-offs with respect to other aspects of
sustainability—for example, costs, animal welfare impacts, and acceptability to consumers.

Sustainability Management Best Practices

The first necessary focal area involves identification and dissemination of environmental
sustainability best management practices in the context of current production norms, specific to
housing system type. The 2012 benchmark LCA of the Canadian egg industry [21] demonstrated
considerable variability in efficiencies among egg farms, with highest variability among producers
using non-cage systems. For example, non-trivial differences in feed conversion efficiencies, rate of lay,
and mortality rates are observed between industry leaders and laggers. Scenarios to assess the life
cycle resource use and emissions mitigation potential of achieving best reported performance for feed
conversion efficiency and rate of lay, as well as sourcing low-impact feeds suggest that further reducing
the resource and emissions intensity of Canadian egg products by over 50% may be possible [21].
Concerted efforts to identify the factors that enable some farms to outperform others—whether
related to management practices, in-place technologies, or other variables (for example, breed of hen),
and programs to mainstream these factors industry-wide may enable substantial improvements in

14
Sustainability 2018, 10, 3524

industry-average performance. Promotion and achievement of best practices would likely improve the
profitability of egg production for individual farmers—in particular, through reducing use of costly
feed and energy inputs. It is unclear, however, what positive or negative animal welfare impacts may
arise, hence any recommended strategies must be carefully assessed on this basis.

Sustainable Feed Sourcing and Formulation

The second priority focal area is feed composition. The largest share of supply chain resource
use and emissions associated with contemporary egg production is attributable to the feeds supplied
to pullets and layers [18,21]. Data collected for the 2012 national benchmark LCA study indicated
considerable diversity in the range and geographical origin of feed inputs from agricultural, livestock,
fisheries, and other production systems [21]. Each feed input that may potentially be sourced for use
in poultry feeds is also characterized by a distinctive life cycle resource use and emissions profile,
with considerable variability between specific feed materials. Each material is similarly distinct in
terms of its nutritional value for poultry, as well as its cost. Feed formulation is currently informed
primarily by nutrition and cost considerations. However, “least environmental cost” feed input
sourcing is the most critical lever for supply chain environmental sustainability management for
egg production. Development of a regionally resolved feed formulation decision support tool that
will integrate nutritional, cost, and environmental impact data for major feed input supply chains
for the Canadian poultry industry is therefore desirable. Integration of nutritional and cost criteria
with environmental impact data is essential, since feed input sourcing recommendations based on
environmental criteria alone may result in feeds that are uneconomical or that result in poor feed
conversion efficiency (hence negating any gains associated with lower environmental cost feed inputs).

Nitrogen Use Efficiency

Nitrogen use efficiency (included, but not limited to, manure management) is the third priority
focal area for environmental sustainability management in this industry [21,56,57]. Nitrogen use
efficiency and loss is important in terms of the net energy, nitrogen, and carbon footprint balance
of egg production, and has important implications for air quality, human and animal health [58].
For farms producing their own feeds and cycling manure nitrogen on-farm, minimizing N loss is
also economically important. Several variables are influential in nitrogen use efficiency and cycling,
such as feed composition, feed conversion efficiency, moisture content of hen excreta, and manure
management strategies [57]. The latter includes collection and handling technologies, residency time
in storage, storage cover, and land application and incorporation methods. Manure belt systems and
manure drying have been proposed as one strategy to reduce losses of nitrogen as ammonia from layer
hen manure, as well as to improve air quality [59]. Implementation of any such technology should
be carefully assessed with respect to the estimated potential systems-level (i.e., life cycle) benefits
and trade-offs, including costs. However, interventions that improve air quality will generally also
improve hen welfare as well as worker health.

Sustainable Intensification Technologies

The fourth priority focal area for improving the environmental performance of egg production is
the identification and implementation of sustainable intensification technologies at farm level. Some
promising sustainable intensification technologies for the egg industry include, for example, those
related to waste valorization, lighting, use of renewable energy sources, and energy-efficient housing.
Each of these will have cost implications, hence consideration of payback time is important. Therefore,
too, is attention to potential hen welfare impacts.
From a “life cycle” perspective, waste valorization represents a significant opportunity for
improving both resource/environmental efficiencies and profitability in the egg industry. While
prior research has underscored the potential limitations and benefits of a subset of relevant waste
valorization opportunities (for example, biogas production from poultry manure) [60–64], current

15
Sustainability 2018, 10, 3524

knowledge regarding the distribution and fate of key waste streams along Canadian egg supply chains,
as well as the comparative efficacy of existing waste valorization technologies is underdeveloped.
Moreover, further research and technology development for novel waste valorization strategies is
needed in support of increased diversion of under-used waste streams including egg shells, mortalities,
and end-of-lay hens. With respect to the latter, the depopulation strategies for hens at end of lay, as
well as potential hen transport requirements if a larger fraction of spent hens are to be processed for
human consumption, will be particularly important from an animal welfare perspective.
Direct energy inputs to layer facilities for lighting, heating, ventilation, and other processes
make a non-trivial contribution to life cycle resource use and emissions for egg production and are
also an important cost of production consideration [18,21]. Similar energy inputs are also required
upstream along egg supply chains for breeder facilities, hatcheries, and pullet facilities. Integration of
renewable energy systems both for layer facilities and along egg supply chains may therefore provide
significant opportunities for improving the life cycle environmental sustainability performance of the
Canadian egg industry. A variety of renewable energy technologies are currently being employed
at a subset of egg production facilities across the country. To date, however, there has been no
systematic accounting of the distribution, scale, feasibility, mitigation potential and scalability of these
technologies for egg production supply chains. With respect to the latter considerations, any such
accounting must necessarily consider geographical and climatic factors including the spatial and
temporal distribution of solar and wind resources to advance regionally appropriate, renewable energy
technology deployment recommendations. Economic costs and payback time need also be considered.
Another area for green technology development and deployment in the egg industry is with
respect to hen housing and other building infrastructure. As much as 30% of greenhouse gas (GHG)
emissions are attributable to the building sector, largely due to energy use over the lifespan of buildings
(UNEP 2009). Net zero energy building technologies aim to create buildings that produce at least as
much renewable energy on site as they consume on an annual basis. Such technologies hence have the
potential to substantially mitigate anthropogenic GHG emissions [65]. Little work has been advanced
to date to evaluate the feasibility and mitigation potential of net zero energy building technologies in
the intensive animal agriculture sector (also a key GHG emitter), where housing is typically employed
for confined poultry, as well as for pork and dairy production. Such production facilities require energy
inputs for lighting, climate control, ventilation, feed delivery, egg collection, manure management, and
sanitation activities. Direct, farm-level energy use for egg production may account for as much as 25%
of cradle-to-farm gate life cycle energy use and GHG emissions [18,21]—depending on farm location,
on-farm efficiencies, and energy sources. Changes to ventilation systems may, however, have negative
impacts on air quality, in turn impacting both worker and hen welfare, and short-term technology
costs must be weighed against long-term returns resulting from energy savings.
Lighting systems for livestock production, in particular for poultry, are influential for animal
health and productivity [66,67]. Diverse lighting systems have been used in the poultry industry.
Most recently, light emitting diode (LED) lighting systems have been developed for poultry
housing. These systems are primarily marketed based on their energy efficiency compared to
competing lighting systems, which can effect significant cost savings for producers. However, several
researchers have reported differences in egg weight, shell strength, rate of lay, bird behavior and feed
conversion efficiency under different single and combined monochromatic LED light regimes [68–70].
Carefully selected LED lighting regimes may therefore have important implications for environmental
sustainability performance which go far beyond direct, farm-level energy savings. This is particularly
true with respect to changes in feed use efficiency, since feed inputs are the largest contributor to both
costs and to supply chain resource use and emissions for egg production [18,21], as well as rate of lay
and mortality rates—both of which influence feed use efficiency. Optimizing LED lighting systems for
sustainability objectives therefore presents an important research area that must necessarily bridge
resource/environmental, economic, and animal welfare considerations.

16
Sustainability 2018, 10, 3524

The current environmental performance profile of the industry largely reflects the production of
eggs by hens in conventional cages. As previously described, slightly superior efficiencies are currently
achieved in cage and enriched cage facilities, reflecting optimization of both management strategies
and genetics for cage-based production in the industry over time. Efficiencies are slightly lower, and
more variable between farms for non-cage systems (for example, with respect to mortality rates) [20].
As the industry transitions away from conventional cage-based production, both farm management
and genetics optimization efforts will be required to close the currently modest efficiency gap between
production in conventional cages and alternative housing systems. This will be similarly important to
maintaining the profitability of egg production. It should be noted, however, that selective breeding
for increased rate of lay looking forward may result in unacceptable welfare trade-offs as a result of
further compromising the skeletal integrity of hens.

3.2.2. Current Challenges and Opportunities with Respect to Regulatory Conditions

Stakeholders Support for Supply Management

If Canadian egg farmers were not to show strong support for supply management, it would
likely be dismantled in a relatively short period of time—in particular, given persistent pressure from
international trading partners such as the United States. The former Canadian Wheat Board is a good
example of the potential consequences of non-unanimous support among farmers—the institution
lost its ability to be the sole purveyor of Western Canadian wheat and barley. Although egg farmers
have and continue to demonstrate strong support for the system, how growth in consumption is
allocated between Canadian regions has caused tensions. For instance, some regions have argued in
the past that they should get greater quota allocation based on their lower cost of production. However,
others argue that since those regions already produce more than they consume, their cost advantage is
cancelled by the cost of transporting eggs long distance. Those tensions have been solved through
negotiations and are currently low.
While challenges exist, supply management continues to find support among Canadians because
they recognize that the system allows farmers to receive adequate compensation for their products,
while also providing consumers with a fair price, and encourages a strong and stable domestic supply.
In addition, unlike the United States and the European Union, which subsidize their producers heavily
and have not been able to control periods of intense overproduction (especially in the dairy sector,
which has led to needless producer suffering and wasted production as well as harmful effects for the
environment) Canada only produces what is required to meet demand [71–73]. Similar to the dairy
industry, the egg industry also suffers when farmers cannot cover their cost of production. In 2013,
for example, French farmers destroyed hundreds of thousands of eggs to protest overproduction
and the subsequent drop in prices [74]. Canada’s system of supply management is not only more
responsible, it is also a more sustainable model because it does not lead to resource wastage and
pollution associated with overproduction. It also fairly compensates workers, who are then able to
support their rural economies and create more vibrant and sustainable rural communities [75]. Doyon
and Bergeron [76] found that investments on farms under supply management in Canada are more
important (excluding quota investments) than those on non-supply-managed farms, because of the
confidence and stability of revenue associated with supply management. Those on-farm investments
also generated more jobs for farms under supply management and the economic impact was mostly
directed towards rural areas.

Supply Management and Animal Welfare

A supply-managed industry is also better equipped to facilitate an orderly transition to
non-conventional cage-based production and may actually support greater innovation given that
producers get predictable and fair returns. This, in turn, encourages experimentation without the same
degree of risk experienced elsewhere [40]. Beyond product innovation and consumer choice, Canada’s

17
Sustainability 2018, 10, 3524

supply-managed egg sector may allow for a smoother transition to alternative housing options
in egg farming because it will, as it becomes mainstream, compensate farmers for the additional
costs of production associated with these more expensive housing alternatives to conventional cages.
The turmoil that was caused when the European Union demanded new housing standards without fair
farmer compensation should serve as a warning against unsupported and uncompensated mandatory
changes in farming practices [74].

3.2.3. Current Challenges and Opportunities with Respect to Social Preferences and
Socio-Economic Conditions

Specialty Eggs and Collective Pricing

The first important economic issue currently facing the Canadian egg industry relates to pricing
along the value chain. The current cost of production formula that is used by EFC to determine
producer egg prices reflects egg production in battery cages. Farmers receive a premium from egg
graders to produce specialty eggs and premiums are negotiated on an individual basis, sometimes
with written contract or sometimes with a verbal agreement. Moreover, retail prices are sometimes at
odds with the cost of production. For example, vitamin D eggs have a premium at retail of roughly 30%
while the cost of production is barely affected. On the other hand, graders take important market risks
while supplying organic eggs, given that they must guarantee a premium to egg farmers to motivate
the capital cost involved, while having little to no guarantees on volume from retailers. Thus, organic
eggs might end up in the regular supply chain, at the sole expense of the grader. As the percentage
of specialty eggs on the market increases, the private nature of premiums might conflict with the
collective principles of supply management. It might also cause problems in gathering sufficient
information for determining the cost of production. How price will be transmitted along the value
chain should also be a concern. Different options are being explored to address this issue. One possible
option is to put at the disposal of farmers contract types for specialty eggs with price information.
This would insure more fairness and reduce the asymmetry of information between graders and
egg farmers. Another option would be, assuming that the growth of specialty eggs will continue, to
have add-on to the cost of production for various types of specialty eggs. For example, organic dairy
producers receive the cost of production plus 22 $ per hectoliter in Québec. This add-on can be revised
on a regular basis using cost items.

Consumer Confidence
The second issue relates to the confidence of consumers in specialty eggs. This has not been an
issue so far in Canada. However, as the variety of specialty eggs increase, how can the consumer be
assured that, for example, the vitamin D and Omega-3 free-range brown eggs purchased are really
what was paid for? Certification is likely to become important in this regard. As an example, Australia
recently experienced a confidence crisis for consumers regarding what free-range implies in the absence
of certification. The situation has also created uncertainty for egg farmers leading to a significant
underproduction of free-range eggs. The increasing prevalence of sustainable sourcing initiatives in the
food sector may also place new burdens on producers with respect to measuring and communicating
around sustainability performance, goals, and progress.
The emergence of specialty eggs implies that attached to the private value of an egg is a social
attribute that can be associated with a public good dynamic. However, even though specific social
attributes are becoming more important for some buyers, preferences are currently heterogeneous
among consumers. This raises interesting issues regarding achieving an appropriate balance between
private and public choice, and whether and to what extent this is best influenced by market forces
and/or regulations. For example, which type of production is best with respect to animal welfare,
the environment, or for workers [22]? At what cost? Interdisciplinary research is required to identify

18
Sustainability 2018, 10, 3524

the appropriate balance between competing attributes, the extent to which stakeholder incentives are
aligned and, in turn, the preferred regulatory or market-based strategy.

Citizens Versus Consumers

The third issue relates to the potential disconnect between the pressure to transition to cage-free
production (largely resulting from lobbying of retailers and fast-food chains in Canada by animal
welfare organizations) and consumer willingness-to-pay for cage-free eggs. As previously mentioned,
cage-free production may actually engender trade-offs with respect to animal welfare, the environment,
workers’ welfare, and economic efficiency. This nuance may be lost on most consumers, who tend to
react adversely to the very idea of cage-based production.
For instance, Doyon et al. [44] found that when presenting consumers with fictive names for
housing systems, the three out of twelves names containing the word cage were by far the ones
considered as the least likely to promote hen welfare. On the other hand, the researchers also found
that when consumers were provided with additional information on the enriched cage system, they
showed increased preference for these eggs relative to regular eggs.
Given that cage-free eggs are readily available but represent less than 10% of the table eggs sold
in Canada, one must naturally wonder about the impact on consumers and on demand for moving
completely to cage-free egg production by 2025. Norwood and Lusk [77] found that consumers were
willing to pay, on average, between 53% and 100% more for cage-free eggs over battery cage eggs.
These results come with important standard deviation, meaning that some participants are not willing
to pay more for cage-free eggs, and in some instances, some would pay less.
California is an interesting example. Cage-free eggs represented less than 10% of consumption in
2008 when a referendum (Proposition 2) to ban battery cages was voted on by 64% of eligible voters.
Malone and Lusk [45] estimate that California’s law banning battery cage increased the retail cost
differential between California and the national egg price average by 51%, while that differential was
historically around 15%. The cost for consumer surplus is estimated by the authors to be between $400
and $850 million.

3.2.4. Current Challenges and Opportunities for Improving Hen Welfare

As previously described, the Canadian egg industry is in the early stages of transitioning away
from housing laying hens in conventional cages. However, to inform the selection of alternative
housing systems, it is critical to understand the animal welfare trade-offs associated with different
housing systems, as well as how these might impact on resource/environmental and socio-economic
sustainability considerations. Rational decision-making must ultimately reflect consideration and
accommodation across these domains.

Ethical Concerns and Scientific Measures

Concerns about animal welfare can be divided into three areas, which form the bases for measures
used in science-based evaluations [78]. These comprise measures of biological function that include
health, mortality, physical condition and production performance and measures of emotional or
affective states of animals that include pain, fear, discomfort, reward, and pleasure. Naturalness,
a third concept of what constitutes a good life for animals, is less amenable to scientific evaluation.
However, it is often defined as the ability to perform natural or species-typical behavior. By quantifying
and comparing the innate drive of animals to perform specific behavior patterns we can determine
what animals want (find rewarding), lending objective measures of affective states to the concept of
naturalness. All three categories of criteria are articulated in most formal definitions of animal welfare,
but it is important to recognize that different stakeholders vary in the degree of importance they place
on the different measures. Farmers and veterinarians tend to value measures of biological function,
animal welfare scientists tend to value measures of subjective states and members of the broader
community value naturalness [78]. In the case of housing systems for laying hens, these criteria are

19
Sustainability 2018, 10, 3524

often conflicting. Public acceptance can drive farming practices, but public perceptions do not always
align with scientific evidence [79].
While most formal definitions of animal welfare include the ability to express “normal” or innate
behavior, the scientific consensus is that it is neither practical nor necessary for hens to be able to
perform all types of behavior [80]. Empirical research has focused on identifying the candidate
behaviors that are most important for hens. Specifically, nesting, perching, foraging, and dustbathing
are considered to be behavioral needs or behavioral priorities [80]. Thus, provision of enough space
and resources to support these behavior patterns are included in most science-based standards.

Welfare Trade-Offs Related to Different Laying Hen Housing Systems

Several literature reviews and scientific reports have summarized findings from studies comparing
the welfare of hens in different housing systems [81–84], including reports comparing various welfare
indicators collected on large-scale commercial farms [85–89]. Generally, all these reports indicate
significant trade-offs for different aspects of welfare for hens in different housing systems. Some
observed differences likely reflect the lesser degree of experience among farmers housing hens in
alternative systems, underscoring the desirability of identifying and disseminating best management
practices with respect to improved welfare outcomes in these systems.
Conventional cages generally result in good health, hygiene, and low mortality, but the lack
of nests, scratch areas and perches coupled with lack of space impose a high degree of behavioral
restriction for hens. Even basic activities such as locomotion, stretching and wing-flapping are
significantly constrained in conventional cages [84]. It is also well established that the lack of load
bearing exercise reduces bone strength of hens.
Hens housed in cage-free systems with nests, perches, and litter (or free-range with access to the
outdoors) have substantial opportunities to perform a greater range of behaviors, but also incur a
significantly greater risk of mortality, injury, and poor health [83,84]. Feather pecking and cannibalism
are major causes of feather loss, poor welfare, and higher mortality, which are mitigated by the
highly controversial practice of beak trimming in many management systems. A recent analysis of
data from 3500 commercial flocks in the EU indicated that mortality rates were significantly higher
and considerably more variable in non-cage and especially in free-range systems compared to cage
systems [89]. In that study, genetic strain of the hen was a significant factor and risks were considerably
greater when hens were not beak trimmed. Smothering, another cause of mortality for hens housed
in large group sizes, occurs when birds mass together and pile on top of one another [90]. Piling can
occur when birds become frightened and panic or when they crowd together at different times of day
to access different resources, for example in communal nests [91] or to dust bathe on litter [92].
Enriched (furnished) cages generally result in production, health, and mortality rates that are
comparable to or better than conventional cages [21,85,86,88]. With more space and added furnishings,
hens in enriched cages have greater opportunities to express motivated behavior than in conventional
cages. Nests in cages are generally well-used and result in hens showing more “settled” (satisfied)
nesting behavior [93]. Perching behavior and/or the increased space and locomotion in enriched cages
results in stronger bones than in conventional cages [94,95]. However, the scratch mats provided in
enriched cages do not fully support foraging or dust bathing behavior [85], and this poses one of the
biggest challenges for full welfare benefits of enriched cages.

Trade-Offs among Welfare, Economics, Environmental Impact and Human Health

Providing hens with greater space allowances increases both building capital costs and operating
costs per dozen eggs produced [96]. Labor costs can be substantially higher, particularly in non-cage
systems. Housing hens in alternative systems can also result in reduced efficiencies from lost product
(damaged eggs in enriched systems and eggs laid outside of the nest in non-cage systems), higher
mortality and reduced feed efficiencies due to energy expenditure related to increased exercise. Poor
feather condition from feather pecking increases bird heat loss which must be compensated by higher

20
Sustainability 2018, 10, 3524

feed intake or supplemental heating of barns [97]. All these factors can increase cost of production and
will also undermine resource efficiency/environmental objectives.
Air quality is also significantly affected by provision of foraging substrate. Higher levels of aerial
dust and microbes compromise hen health and worker health and safety [98,99]. Emissions of ammonia
and particulate matter from barns may also increase risks to public health [100]. Developing means for
mitigating air quality issues inherent in non-cage systems is an important area for future research.
Genetic selection for increased egg production has also come at the expense of hen health and
welfare. The demand for calcium to support shell formation of the large numbers of eggs that modern
layers produce results in poor skeletal health manifested as osteoporosis, fragile bones, and subsequent
risks for bone breakage [101]. Despite advances in nutrition to support the calcium and phosphorus
requirements of hens, a major portion of the calcium required for egg formation comes from the hen’s
skeleton which progressively weakens over her lifetime. Osteoporosis is exacerbated by restricted
housing and the lack of load bearing exercise. However, although opportunities for exercise in enriched
and non-cage housing do result in stronger bones, the skeleton of the modern laying is still relatively
weak and increased freedom of movement also increases risks for bone fractures from collisions with
furnishings. The keel bone (sternum) is particularly susceptible to fractures and prevalence rates have
been reported to range from 10 to 30% in conventional cages, 20 to 60% in enriched cages and greater
than 85% in non-cage systems [102]. Genetic selection for improved bone strength may provide a
solution, although there appears to be an inverse relationship between production traits (egg number
and shell quality) and bone strength.
Huge gains can be made for not only improving hen welfare and but also reducing loss in
resource efficiencies by refining system design (technology) and optimizing nutrition, genetics, and
management of alternative housing systems. The large degree of variability found in the literature
(e.g., [89]) highlights the potential for non-cage systems to perform well. Research aimed at improving
system design, with regards to hens being able to navigate the system without injury, and to readily use
nests is essential. Performance testing combined with genome-wide DNA marker analyses are proving
valuable tools for genetic selection that balances production and feed efficiency, skeletal integrity and
the behavioral traits (i.e., use of nests and reductions in feather pecking) necessary for improving
efficiencies and hen welfare in non-cage systems [103].

4. Synthesis and Conclusions

Based on our analysis of historical trends and current regulatory and socio-economic conditions,
we identify several major challenges for or threats to the sustainability of the egg industry, along with
a variety of alternative strategies to resolve them. We further posit that resolution of these challenges
must be supported not only by interdisciplinary research but also by knowledge transfer to enable
reconciliation of potential trade-offs between alternative courses of action.
These identified challenges largely relate to shifting consumer and other stakeholder preferences
and expectations, which create pressures on egg producers to adapt their practices to produce eggs in
particular ways and with particular attributes [104]. It should be underscored that such preferences
may not be sufficiently knowledge-based, nor sufficiently informed of potential trade-offs. Foremost
among these is the current pressure to transition from cage to non-cage housing systems, based on
animal welfare considerations. In a recent survey, US consumers were asked to indicate whether
moving from conventional to cage-free housing would have none, positive or negative impact on hen
health, hen behavior, natural resource use efficiency, worker health and safety, food safety and egg
quality [79]. Well over 50% and upwards of 70% of respondents indicated positive impacts for all the
various attributes, respectively, although scientific evidence indicates either no or negative impacts for
all of them.
There are distinctive trade-offs with respect to welfare outcomes, with different housing systems
variously providing for superior or poorer outcomes, depending on the specific measure considered.
At the same time, alternative housing systems imply different resource efficiency/environmental

21
Sustainability 2018, 10, 3524

sustainability outcomes. Performance in non-cage systems is currently more variable and somewhat
poorer than conventional and enriched colony cage-based production, hence research and development
of technology and management strategies to optimize production in alternative housing systems is
highly recommended. Perhaps more important is the transfer of research and practical knowledge
to farmers transitioning to these new housing and management systems. It is well established that
the knowledge, skills, attitudes, and beliefs of the stock people caring for livestock and poultry have
profound effects on welfare and production performance of the animals in their care. Training can be
used to increase knowledge, change attitudes, and improve performance. While many farmers move
from managing simpler to more complex housing systems, a steep learning curve can be expected,
with performance and efficiencies continuously improving as they did for conventional cages. Since
many farmers may view the transition as being forced upon them, their attitudes about the systems
may be negative and may also need to evolve with experience [105,106].
One strategy that has been tested in the UK is the development of comprehensive animal welfare
assessments and benchmarking tools combined with feedback and educational materials for farmers.
This top-down approach can be delivered within quality assurance schemes or as industry-wide
initiatives and involve scientists, veterinarians, government extension specialists and various industry
stakeholders. One example is Assurewel [107], a 6-year collaboration among the University of Bristol,
RSPCA, and the Soil Association of the UK. As part of this, the FeatherWel project [108] specifically
aimed to reduce injurious pecking on UK farms by providing an assessment tool that farmers could
use to measure and track feather condition in their flocks together with advice on practical strategies
to prevent the problem. Mullan et al. [109] reported that 59% of the 662 UK farmers involved in
the project made management changes to improve welfare during the first year of the program, and
there was a significant reduction in feather loss from year 1 to year 2. Another approach tested
more broadly in the EU as part of the Horizon 2020 EU Research and Innovation program was the
Hennovation project [110]. Hennovation also targeted solutions to feather pecking but by developing
and disseminating technical innovations using “practice-driven innovation networks” comprising
farmers, scientists, veterinarians and farm advisors. Management practices were developed and tested
on farms by farmers and the results shared through on-line training, web-based tools and facilitated
sessions [111].
In Canada, improvements in both animal welfare and resource use efficiency could be realized by
combining efforts for development, knowledge transfer and implementation of best practices for both
aspects of sustainability together. The infrastructure and resources of the supply management system
could support the framework for such an approach. Currently, a feather scoring system for Canadian
egg producers has been distributed through the provincial boards as part of an epidemiological study
and benchmarking exercise [112].
The transition to alternative housing systems also presents challenges for Canadian producers
from an economic stand-point, which can be partially remedied through the development of cost of
production formulas that ensure a fair return to producers within the supply-managed industry. Such
a development will serve to reduce risk for both producers and graders, and provide more predictable
prices for consumers.
The continued rise of sustainable sourcing as a management consideration for agri-food supply
chains, along with generally increasing expectations for accountability and transparency with respect
to sustainability management, reporting, and demonstration of improvement, will also likely challenge
the egg industry to respond accordingly. From a logistical perspective, it is imperative that farmers be
enabled to participate in related initiatives in a non-burdensome manner. This will require development
of rigorous sustainability measurement and reporting tools that are both transparent and easy to use.
It must be anticipated that multi-criteria sustainability reporting tools that incorporate a combination
of environmental, animal welfare, economic, and other indicators will likely highlight the inevitability
of trade-offs associated with different management or technology alternatives for the industry. With
respect to improvement opportunities, a variety of technology and management options are available

22
Sustainability 2018, 10, 3524

that may improve environmental sustainability outcomes, but each must be simultaneously evaluated
with respect to potential negative impacts on animal welfare and cost of production.
Another persistent threat to industry sustainability is pressure to dismantle the supply
management system that currently governs egg production in Canada. This would likely precipitate
consolidation and vertical integration in the industry, with many/most of the currently 1000+ farms
disappearing. The opening up of the Canadian market to US egg imports would also likely considerably
reduce domestic production.
Loss of supply management would also potentially undermine the ability to orchestrate a
smooth transition to alternative housing systems in the Canadian egg industry. There is need
for further research to understand potential welfare and sustainability trade-offs of production
in supply-managed versus non-supply-managed contexts. Although conventional economic logic
would predict higher efficiencies under free market conditions, data suggest similar feed conversion
efficiency between US and Canadian flocks but higher mortality rates for US layers (6.7% mortality
rate reported for the US for 2010 for conventional cage production, compared to 3.2% for Canada
in 2012). However, the concentration of egg production in the US in grain-producing areas creates
higher transport-related efficiencies compared to the nationally distributed production (which often
necessitates more transportation of feed inputs) characteristic of the Canadian supply-managed
industry. At the same time, distributed production reduces the need for more higher impact,
refrigerated transport and, potentially, food waste.
There are also a variety of existential threats to the industry that merit consideration. Managing
for the future is clearly fraught with uncertainties. Nonetheless, a subset of additional challenges
that the egg industry will almost certainly grapple with can be identified with some measure of
confidence. First, the growing awareness of the centrality of the agri-food system (in particular,
the livestock sector) to many of our most pressing sustainability concerns points towards increased
competition for legitimacy in the food space looking forward. Indeed, this is underscored by the rapid
emergence and proliferation of sustainable sourcing schemes for agri-food products, largely driven by
food processors, retailers, and fast-food chains. Grace of the nutritional value of eggs (currently the
reference product for nutritional quality in broadly accepted measures such as Protein Digestibility
Corrected Amino Acid Scores (PDCAAS) and Dietary Indispensable Amino Acid Scores (DIAAS)),
as well as the relative efficiency of producing poultry compared to swine and ruminants, the egg
industry is relatively advantaged at the outset. Nonetheless, it would be both prudent and strategic
for the industry to be proactive with respect to positioning in this regard—in particular with respect to
actively communicating around the coupled nutritional and sustainability benefits of eggs. This may
also prove important considering growing markets for alternatives to animal products, including egg
replacement products.
Second, projected growth in food production globally will only serve to exacerbate competition
for land, energy, water, and other resources, as well as further disrupt global biogeochemical cycles
and systems including the nitrogen and phosphorus cycles and the global climate system. The egg
industry will likely be impacted by these changes at multiple levels. This includes emerging regulatory
responses which may require operational and technological changes within the industry, potential cost
increases for inputs such as feed and energy, greater uncertainty associated with yields along feed
input supply chains and increased extreme weather events (and associated heating and ventilation
challenges). These phenomena will create sustainability risks and opportunities. It is incumbent on the
industry, at the leadership level, to remain attentive and to respond nimbly and effectively to such
risks and opportunities as they emerge.
A third wild card for the egg industry is the extent to which disruptive technologies may alter both
perceptions and norms regarding the production and consumption of food. For example, emerging
technologies such as 3D printing of food will enable precision nutrient delivery, tailored to individual
dietary needs and preferences, as well as incorporation on non-traditional protein alternatives such as

23
Sustainability 2018, 10, 3524

insect protein. Against this backdrop, positioning of traditional foods such as eggs in the food space
based on nutritional attributes may enjoy diminishing returns.
More directly relevant to the egg industry will be growth of the in-vitro biomass and animal
product replacements sectors. Since the widely publicized creation of the first lab-grown beef burger
in 2013, research, investment, and commercial development in this emerging disruptor sector has
burgeoned. Cultured animal products may redefine how we think about, produce, and consume
animal protein in the future. While clearly directly competitive with beef, pork, and chicken in the
near to medium term, comparable advances in producing cultured egg and dairy substitutes are also
likely over time. More directly relevant to the egg industry are vegan and vegetarian egg replacement
products, which may have lower resource and environmental impacts as well as eliminate animal
welfare-related concerns.
In short, the egg industry faces multiple risks and opportunities from a sustainability perspective
in the coming years. Some are immediate and tangible, others less certain with respect to probability,
magnitude, and consequence. Supporting the egg industry in successfully navigating this future
will require effective research on multiple fronts and, in many cases, interdisciplinary research and
knowledge mobilization that draws on the perspectives, tools, and competencies of multiple research
areas to recognize and navigate inevitable trade-offs.

Author Contributions: All authors contributed to the conception, research and writing of this manuscript.
Funding: Funds for publication costs are provided by the Natural Sciences and Engineering Research Council of
Canada/Egg Farmers of Canada Industrial Research Chair in Sustainability (Pelletier). This research received no
external funding.
Acknowledgments: The research chairs held by Pelletier, Doyon, Muirhead and Widowski are each supported by
Egg Farmers of Canada.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Pelletier, N.; Tyedmers, P. Forecasting potential global environmental costs of livestock production 2000–2050.
Proc. Natl. Acad. Sci. USA 2010, 107, 18371–18374. [CrossRef] [PubMed]
2. Foley, J.; Ramankutty, N.; Brauman, K.; Cassidy, E.; Gerber, J.; Johnston, M.; Mueller, N.; O’Connel, C.;
Ray, D.; West, P.; et al. Solutions for a cultivated planet. Nature 2011, 478, 337–342. [CrossRef] [PubMed]
3. Rockström, J.; Williams, J.; Daily, G.; Noble, A.; Matthews, N.; Gordon, L.; Wetterstrand, H.; DeClerck, F.;
Shah, M.; Steduto, P.; et al. Sustainable intensification of agriculture for human prosperity and global
sustainability. Ambio 2017, 46, 4–17. [CrossRef] [PubMed]
4. Pelletier, N. Life cycle thinking, measurement and management for food system sustainability. Environ. Sci.
Technol. 2015, 49, 7515–7519. [CrossRef] [PubMed]
5. Pretty, J.; Toulmin, C.; Williams, S. Sustainable intensification in African agriculture. Int. J. Agric. Sustain.
2011, 9, 5–24. [CrossRef]
6. Sala, S.; Farioli, F.; Zamagni, A. Progress in sustainability science: Lessons learnt from current methodologies
for sustainability assessment: Part 1. Int. J. Life Cycle Assess. 2013, 18, 1653–1672. [CrossRef]
7. McClelland, S.; Arndt, C.; Gordon, D.; Thoma, G. Type and number of environmental impact categories used
in livestock life cycle assessment: A systematic review. Livest. Sci. 2018, 209, 39–45. [CrossRef]
8. Garnett, T. Three perspectives on sustainable food security: Efficiency, demand restraint, food system
transformation. what role for life cycle assessment? J. Clean. Prod. 2014, 73, 10–18. [CrossRef]
9. Kennard, D.C. The trend toward confinement in poultry production. Poult. Sci. 1928, 8, 23–28.
10. Lee, C.E. Profitable Broiler Battery and Layer Cage Management, 6th ed.; Beacon Milling Co., Inc.: Cayuga, NY,
USA, 1951.
11. Hanke, O.A.; Skinner, J.L.; Florea, J.H. Chronology: American Poultry History. In American Poultry History
(1823–1973); American Printing and Publishing Inc.: Madison, WI, USA, 1974; pp. 680–741.
12. Freidberg, S.E. The Triumph of the Egg. Comp. Stud. Soc. Hist. 2008, 50, 400–423. [CrossRef]

24
Sustainability 2018, 10, 3524

13. Hartman, R. Keeping Chickens in Cages: A Description of the Outdoor Individual Cage System of Poultry
Management as Developed Mainly in Southern California; Pacific Poultryman: Palo Alto, CA, USA, 1950;
p. 11.
14. Brambell, F. Report of the Technical Committee to Enquire into the Welfare of Animals Kept under Intensive Livestock
Husbandry Systems; Her Majesty’s Stationery Office: London, UK, 1965.
15. Shaver Poultry. The Shaver Heritage Story. Available online: https://www.shaver-poultry.com/en/about-
us/history/ (accessed on 12 August 2018).
16. Siegel, P.; Dodgson, J.; Andersson, L. Progress from chicken genetics to the chicken genome. Poult. Sci. 2006,
85, 2050–2060. [CrossRef] [PubMed]
17. Sharma, B. Poultry production, management, and bio-security measures. J. Agric. Environ. 2010, 11, 120–125.
[CrossRef]
18. Pelletier, N.; Ibarbaru-Blanc, M.; Xin, H. Comparison of the U.S. egg industry’s environmental footprint in
1960 and 2010. Poult. Sci. 2014, 93, 243–255.
19. StatsCan. Production and Disposition of Eggs, Annual. Table: 32-10-0119-01 (Formerly CANSIM 003-0020).
Available online: https://www150.statcan.gc.ca/t1/tbl1/en/cv.action?pid=3210011901 (accessed on 12
August 2018).
20. Pelletier, N. Changes in the life cycle environmental footprint of egg production in Canada from 1962–2012.
J. Clean. Prod. 2018, 176, 1144–1153. [CrossRef]
21. Pelletier, N. Life cycle assessment of Canadian egg products, with differentiation by hen housing system
type. J. Clean. Prod. 2017, 152, 167–180. [CrossRef]
22. Mollenhorst, H.; Berentsen, P.; de Boer, I. On-farm quantification of sustainability indicators: An application
to egg production systems. Br. Poult. Sci. 2006, 47, 405–417. [CrossRef] [PubMed]
23. Cederberg, C.; Sonesson, U.; Henriksson, M.; Sund, V.; Davis, J. Greenhouse Gas Emissions from Swedish
Production of Meat, Milk and Eggs 1990 and 2005; SIK Report 793; Swedish Institute for Food and Biotechnology:
Gothenberg, Sweden, 2009.
24. Wiedemann, S.; McGahan, E. Environmental Assessment of an Egg Production Supply Chain Using Life Cycle
Assessment; Australian Egg Corporation Limited: North Sydney, Australia, 2011.
25. Leinonen, I.; Willaims, A.; Wiseman, J.; Guy, J.; Kyriazakis, I. Predicting the environmental impacts of chicken
systems in the United Kingdom through a life cycle assessment: Egg production systems. Poult. Sci. 2012,
91, 26–40. [CrossRef] [PubMed]
26. Pelletier, N.; Ibarbaru-Blanc, M.; Xin, H. Life cycle assessment of greenhouse gas emissions for contemporary
intensive egg production systems in the Upper Midwestern United States. J. Clean. Prod. 2013, 54, 108–114.
[CrossRef]
27. Ghasempour, A.; Ahmadi, E. Assessment of environmental impacts of egg production chain using life cycle
assessment. J. Environ. Manag. 2016, 183, 980–987. [CrossRef] [PubMed]
28. Poultry Keeping on the Modern Farm. Can. Poult. J. 1931, 6, 85.
29. Decades: A look back through the last 100 years of Canadian Poultry. Can. Poult. Mag. 2013, 100, 32.
Available online: https://www.canadianpoultrymag.com/100th-anniversary/key-developments/decades-
13025 (accessed on 7 June 2018).
30. Harkness, D. Memorandum to Cabinet re Eggs. LAC, MG32 B 40 46, B 20S, File 6-3-8 Eggs (General)
1957–1963; 1959. Available online: http://data2.archives.ca/pdf/pdf001/p000000590.pdf (accessed on
30 September 2018).
31. Skogstad, G. The Politics of Agricultural Policy-Making in Canada; University of Toronto Press: Toronto, ON,
Canada, 1987.
32. Ferries, C. Integration: The basic differences between vertical integration and contractual farming.
Can. Poultrym. 1961, 8, 26–27.
33. CDA’s Poultry Director Looks at Marketing Boards. Can. Poultrym. 1966, 1, 31.
34. Bushfield, E. Should We Socialize the Poultry Industry. Can. Poultrym. 1941, 2, 15.
35. Canadian Egg Marketing Agency. First Annual Report of the Canadian Egg Marketing Agency for Presentation to
Minister of Agriculture Canada, The Honourable E. F. Whelan, National Farm Products Marketing Council and First
Annual Public Meeting; Canadian Egg Marketing Agency: Ottawa, ON, Canada, 1974; pp. 2–3.
36. Scott, J. The more they lay, the poorer you get. The Globe and Mail, 5 January 1972; 25.
37. Elizabeth Thompson Advises: Budget, don’t boycott, woman says. The Globe and Mail, 2 January 1967; p. 12.

25
Sustainability 2018, 10, 3524

38. Stephens, D. Processors, retailers advise marketing boards: Farmers sow cooperation to reap increased
profits. The Globe and Mail, 7 March 1967; p. B5.
39. Egg Marketing Agency. Proposal for a National Egg Marketing Plan for Canada; RG 17, Vol 3765, File 611.9E1,
Part 3; Agric Poultry Others; Egg Marketing Agency: Ottawa, ON, Canada, 1972.
40. Tamini, L.; Doyon, M.; Zan, M. Investment behavior of Canada egg producers: Analyzing the impacts of
change in risk aversion and in the variability of eggs prices and production costs. Br. Food J. 2018, 120, 96–107.
[CrossRef]
41. Consumer Price Index. Agriculture and Agri-Food Canada. Available online: http://www.agr.gc.ca/
eng/industry-markets-and-trade/canadian-agri-food-sector-intelligence/poultry-and-eggs/poultry-
and-egg-market-information/industry-indicators/consumer-price-index/?id=1384971854414 (accessed
on 28 September 2018).
42. Per capita Disappearance. Agriculture and Agri-Food Canada. Available online: http://www.agr.gc.ca/
eng/industry-markets-and-trade/canadian-agri-food-sector-intelligence/poultry-and-eggs/poultry-
and-egg-market-information/industry-indicators/per-capita-disappearance/?id=1384971854413 (accessed
on 28 September 2018).
43. Doyon, M.; Bergeron, S. Understanding strategic behaviour and its contribution to hypothetical bias when
eliciting values for a private good. Can. J. Agric. Econ. 2016, 64, 653–666. [CrossRef]
44. Doyon, M.; Bergeron, S.; Crandfield, J.; Tamini, L.; Criner, G. Consumer preferences for improved hen
housing: Is a cage a cage? Can. J. Agric. Econ. 2016, 64, 739–751. [CrossRef]
45. Malone, T.; Lusk, J. Putting the chicken before the egg price: An ex post analysis of California’s battery cage
ban. J. Agric. Resour. Econ. 2016, 41, 518–532.
46. Brady, T. Britons Debate Which Comes First: The Egg or the Hen’s Happiness. The New York Times, 5 August
1953; p. 17.
47. Lewis, H.R. America’s Debt to the Hen. Natl. Geogr. 1927, 51, 453–467.
48. Harrison, R. Animal Machines: The New Factory Farming Industry; Vincent Stuart Publishers Ltd.: London, UK,
1964; p. 186.
49. Appleby, M.C. The European Union ban on conventional cages for laying hens: History and prospects.
J. Appl. Anim. Welf. Sci. 2003, 6, 103–121. [CrossRef] [PubMed]
50. Council Directive 1999/74/EC Laying Down Minimum Standards for the Protection of Laying Hens. Off. J.
Eur. Community 1999, L203, 53–57. Available online: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?
uri=OJ:L:1999:203:0053:0057:EN:PDF (accessed on 15 August 2018).
51. National Farm Animal Care Council. Brief History of the Codes; National Farm Animal Care Council (NFACC):
Lacombe, AB, Canada. Available online: http://www.nfacc.ca/brief-history-of-the-codes (accessed on
15 August 2018).
52. National Farm Animal Care Council. Code of Practice for the Care and Handling of Pullets and Laying Hens;
National Farm Animal Care Council (NFACC): Lacombe, AB, Canada, 2017. Available online: http://www.
nfacc.ca/poultry-layers-code-of-practice (accessed on 15 August 2018).
53. Mench, J.; Sumner, D.; Rosen-Molina, J. Sustainability of egg production in the United States—The policy
and market context. Poult. Sci. 2011, 90, 229–240. [CrossRef] [PubMed]
54. Kaufman, M. McDonald’s tells farmers to treat chickens better. The Washington Post. 23 August 2000.
Available online: https://www.washingtonpost.com/archive/politics/2000/08/23/mcdonalds-tells-
farmers-to-treat-chickens-better/e03b291a-d563-4321-b14e-57ec73338952/?noredirect=on&utm_term=
.8fa99c27445b (accessed on 15 August 2018).
55. Shields, S.; Shapiro, P.; Rowan, A. A decade of progress toward ending the confinement of farm animals in
the United States. Animals 2017, 7, 40. [CrossRef] [PubMed]
56. Retail Council of Canada Grocery Members Voluntarily Commit to Course Cage-Free; Retail Council of Canada:
Toronto, ON, Canada, 2016; Available online: https://www.retailcouncil.org/media/newsreleases/retail-
council-of-canada-grocery-members-voluntarily-commit-to-source-cagefree (accessed on 15 August 2018).
57. Gerber, P.; Uwizeye, A.; Shulte, R.; Opio, C.; de Boer, I. Nutrient use efficiency: A valuable approach to
benchmark the sustainability of nutrient use in global livestock production? Curr. Opin. Environ. Sustain.
2014, 9–10, 122–130. [CrossRef]

26
Sustainability 2018, 10, 3524

58. Westhoek, H.; Lesschen, J.; Leip, A.; Rood, T.; Wagner, S.; De Marco, A.; Murphy-Bokern, D.; Pallière, C.;
Howard, C.; Oenema, O.; et al. Nitrogen on the Table: The Influence of Food Choices on Nitrogen Emissions and the
European Environment; Centre for Ecology & Hydrology, European Nitrogen Assessment Special Report on
Nitrogen and Food: Edinburgh, UK, 2015.
59. Ghaly, A.; Alhattab, M. Drying poultry manure for pollution potential reduction and production of organic
fertilizer. Am. J. Environ. Sci. 2013, 9, 88–102. [CrossRef]
60. De Meester, S.; Demeyer, J.; Velge, F.; Peene, A.; Van Lanenhove, H.; Dewulf, J. The environmental
sustainability of anaerobic digestion as a biomass valorization technology. Bioresour. Technol. 2012, 121,
396–403. [CrossRef] [PubMed]
61. Billen, P.; Costa, J.; Van der Aa, L.; Van Caneghem, J.; Vandecasteele, C. Electricity from poultry manure: A
cleaner alternative to direct land application. J. Clean. Prod. 2015, 96, 467–475. [CrossRef]
62. Fernandez-Lopez, M.; Puig-Gamero, M.; Lopez-Gonzalez, D.; Avalos-Ramirez, A.; Valverde, J.;
Sanchez-Silva, L. Life cycle assessment of swine and dairy manure: Prolysis and combustion processes.
Bioresour. Technol. 2015, 182, 184–192. [CrossRef] [PubMed]
63. Hajjaji, N.; Houas, A.; Pons, M.-N. Thermodynamic feasibility and life cycle assessment of hydrogen
production via reforming poultry fat. J. Clean. Prod. 2016, 134, 600–612. [CrossRef]
64. Molins, G.; Alvarez, M.; Garrido, N.; Macanas, J.; Carrillo, F. Environmental impact assessment of polylactide
(PLA)/chicken feathers biocomposite materials. J. Polym. Environ. 2018, 26, 873–884. [CrossRef]
65. United Nations Environment Program. Buildings and Climate Change: Summary for Decision-Makers; United
Nations Environment Program Sustainable Buildings Initiative, United Nations Environment Program:
Nairobi, Kenya, 2009.
66. Er, D.; Wang, Z.; Cao, J.; Chen, Y. Effect of monochromatic light on the egg quality of laying hens. J. Appl.
Poult. Res. 2007, 16, 605–612. [CrossRef]
67. Hassan, M.; Sultana, S.; Choe, H.; Ryu, K. Effect of combinations of monochromatic LED light color on the
performance and behavior of laying hens. J. Poult. Sci. 2014, 51, 321–326. [CrossRef]
68. Karakaya, M.; Parlat, S.; Yilmaz, M.; Yildirm, I.; Ozalp, B. Growth performance and quality properties of
meat from broiler chickens reared under different monochromatic light sources. Br. Poult. Sci. 2009, 50,
76–82. [CrossRef] [PubMed]
69. Huber-Eicher, B.; Suter, A.; Spring-Stahli, P. Effects of colored light-emitting diode illumination on behavior
and performance of laying hens. Poult. Sci. 2013, 92, 869–873. [CrossRef] [PubMed]
70. Mendes, A.; Paixao, S.; Restelatto, R.; Morello, G.; de Moura, D.; Possenti, J. Performance and preference of
broiler chickens exposed to different lighting sources. J. Appl. Poult. Res. 2013, 22, 62–70. [CrossRef]
71. Hornby, C.; Felix, B. Europe’s farmers dump milk to protest low prices. Reuters. 16 September 2009.
Available online: https://www.reuters.com/article/us-europe-dairy-protests/europes-farmers-dump-
milk-to-protest-low-prices-idUSTRE58F4KG20090916 (accessed on 5 August 2018).
72. Hadden, H. Got milk? Too much of it, say US dairy producers. The Wall Street Journal. 20 May
2017. Available online: https://www.wsj.com/articles/got-milk-too-much-of-it-say-u-s-dairy-farmers-
1495278002 (accessed on 5 August 2018).
73. Dillon, J. Got too much milk? dairy dumping highlights production bottlenecks, Northeast surplus. Vermont
Public Radio. 9 May 2018. Available online: http://digital.vpr.net/post/got-too-much-milk-dairy-dumping-
highlights-production-bottlenecks-northeast-surplus#stream/0 (accessed on 5 August 2018).
74. EU blamed for French Egg Crisis. Euractiv. 13 August 2013. Available online: https://www.euractiv.com/
section/agriculture-food/news/eu-blamed-for-french-egg-crisis/ (accessed on 5 August 2018).
75. Supply management benefits farmers, rural economy. Western Producer. 9 July 2015. Available online:
https://www.producer.com/2015/07/supply-management-benefits-farmers-rural-economy/ (accessed
on 5 August 2018).
76. Doyon, M.; Bergeron, S. Economic Impact from Farm Investments in Canada; Project Report, CIRANO, 2018RP-12;
CIRANO: Quebec, QC, Canada, 2018.
77. Norwood, B.; Lusk, J. A calibrated auction-conjoint valuation method: Valuing pork and egg produced
under differing animal welfare conditions. J. Environ. Econ. Manag. 2011, 62, 80–94. [CrossRef]
78. Fraser, D.; Weary, D.; Pajor, E.; Milligan, B. A scientific conception of animal welfare that reflects ethical
concerns. Animal Welfare 1997, 6, 187–205.

27
Sustainability 2018, 10, 3524

79. Ochs, D.; Wolf, C.; Widmar, N.; Bir, C. Consumer perceptions of egg-laying hen housing systems. Poult. Sci.
2018, 97, 3390–3396. [CrossRef] [PubMed]
80. Weeks, C.; Nicol, C. Behavioural needs, priorities and preferences of laying hens. World’s Poult. Sci. J. 2006,
62, 296–307. [CrossRef]
81. Scientific Panel on Animal Health and Welfare. Welfare aspects of various systems for keeping laying hens.
EFSA J. 2005, 197, 1–23. Available online: https://efsa.onlinelibrary.wiley.com/doi/pdf/10.2903/j.efsa.2005.
197 (accessed on 15 August 2018).
82. LayWel. Welfare Implications of Changes in Production Systems for Laying Hens: Deliverable 7.1 Overall
Strengths and Weaknesses of Each Defined Housing System for Laying Hens, and Detailing the Overall
Welfare Impact of Each Housing System. 2006. Available online: http://www.laywel.eu/web/pdf/
deliverable%2071%20welfare%20assessment.pdf (accessed on 15 August 2018).
83. Lay, D.; Fulton, R.; Hester, P.; Karcher, D.; Kjaer, J.; Mench, J.A.; Porter, R. Hen welfare in different housing
systems. Poult. Sci. 2011, 90, 278–294. [CrossRef] [PubMed]
84. Widowski, T.; Classen, H.; Newberry, R.; Petrik, M.; Schwean-Lardner, K.; Yue Cottee, S.; Cox, B. Code of
Practice for the Care and Handling of Pullets, Layers and Spent Fowl: Review of Scientific Research on Priority Issues;
National Farm Animal Council: Lacombe, AB, Canada, 2013. Available online: https://www.nfacc.ca/
resources/codes-of-practice/poultry-layers/Layer_SCReport_2013.pdf (accessed on 25 September 2018).
85. Rodenburg, T.; Tuyttens, F.; De Reu, K.; Herman, L.; Zoons, J.; Sonck, B. Welfare assessment of laying hens in
furnished cages and non-cage systems: An on-farm comparison. Anim. Welf. 2008, 17, 363–373.
86. Sherwin, C.; Richards, G.; Nicol, C. Comparison of the welfare of layer hens in 4 housing systems in the UK.
Br. Poult. Sci. 2010, 51, 488–499. [CrossRef] [PubMed]
87. Petrik, M.; Guerin, M.; Widowski, T. On-farm comparison of keel fracture prevalence and other welfare
indicators in conventional cage and floor-housed laying hens in Ontario, Canada. Poult. Sci. 2015, 94,
579–585. [CrossRef] [PubMed]
88. Blatchford, R.; Fulton, R.; Mench, J. The utilization of the Welfare Quality® assessment for determining
laying hen condition across three housing systems. Poult. Sci. 2016, 95, 154–163. [CrossRef] [PubMed]
89. Weeks, C.; Lambton, S.; Williams, A. Implications for welfare, productivity and sustainability of the variation
in reported levels of mortality for laying hen flocks kept in different housing systems: A meta-analysis of ten
studies. PLoS ONE 2016, 11, e0146394. [CrossRef] [PubMed]
90. Barrett, J.; Rayner, A.; Gill, R.; Willings, T.; Bright, A. Smothering in UK free-range flocks. Part 1: Incidence,
location, timing and management. Vet. Rec. 2014, 175, 19. [CrossRef] [PubMed]
91. Bright, A.; Johnson, E. Smothering in commercial free-range laying hens: A preliminary investigation.
Vet. Rec. 2011, 168, 512. [CrossRef] [PubMed]
92. Campbell, D.; Makagon, M.; Swanson, J.; Siegford, J. Litter use by laying hens in a commercial aviary: Dust
bathing and piling. Poult. Sci. 2016, 95, 164–175. [CrossRef] [PubMed]
93. Hunniford, M.; Widowski, T. Curtained nests facilitate settled nesting behaviour of laying hens in furnished
cages. Appl. Anim. Behav. Sci. 2018, 202, 39–45. [CrossRef]
94. Jendral, M.; Korver, D.; Church, J.; Feddes, J. Bone mineral density and breaking strength of white leghorns
housed in conventional, modified, and commercially available colony battery cages. Poult. Sci. 2008, 87,
828–837. [CrossRef] [PubMed]
95. Casey-Trott, T.; Korver, D.; Guerin, M.; Sandilands, V.; Torrey, S.; Widowski, T. Opportunities for exercise
during pullet rearing, Part II: Long-term effects on bone characteristics of adult laying hens at the end-of-lay.
Poult. Sci. 2017, 96, 2518–2527. [CrossRef] [PubMed]
96. Matthews, W.; Sumner, D. Effects of housing system on the costs of commercial egg production. Poult. Sci.
2014, 94, 552–557. [CrossRef] [PubMed]
97. Peguri, A.; Coon, C. Effect of feather coverage and temperature on layer performance. Poult. Sci. 1993, 72,
1318–1329. [CrossRef]
98. David, B.; Mejdell, C.; Michel, V.; Lund, V.; Moe, R. Air quality in alternative housing systems may have an
impact on laying hen welfare. Part II—Ammonia. Animals 2015, 5, 886–896. [CrossRef] [PubMed]
99. Zhao, Y.; Shepherd, T.; Li, H.; Xin, H. Environmental assessment of three egg production systems–Part I:
Monitoring system and indoor air quality. Poult. Sci. 2015, 94, 518–533. [CrossRef] [PubMed]

28
Sustainability 2018, 10, 3524

100. Shepherd, T.; Zhao, Y.; Li, H.; Stinn, J.; Hayes, M.; Xin, H. Environmental assessment of three egg production
systems—Part II. Ammonia, greenhouse gas, and particulate matter emissions. Poult. Sci. 2015, 94, 534–543.
[CrossRef] [PubMed]
101. Widowski, T.; Casey-Trott, T.; Hunniford, M.; Morrissey, K. Welfare of laying hens: An overview. In Achieving
Sustainable Production of Eggs Volume 2: Animal Welfare and Sustainability; Roberts, J.R., Ed.; Burleigh Dodds
Series in Agricultural Science (Book 17); Burleigh Dodds Science Publishing: Cambridge, UK, 2017.
102. Harlander-Matauschek, A.; Rodenburg, T.; Sandilands, V.; Tobalske, B.W.; Toscano, M. Causes of keel bone
damage and their solutions in laying hens. World’s Poult. Sci. J. 2015, 71, 461–472. [CrossRef]
103. Preisinger, R. Innovative layer genetics to handle global challenges in egg production. Br. Poult. Sci. 2018, 59,
1–6. [CrossRef] [PubMed]
104. Swanson, J.; Lee, Y.; Thompson, P.; Bawden, R.; Mench, J. Integration: Valuing stakeholder input in setting
priorities for socially sustainable egg production. Poult. Sci. 2011, 90, 2110–2121. [CrossRef] [PubMed]
105. Hemsworth, P. The human factor: Influence on livestock performance and welfare. Proc. N. Z. Soc. Anim.
Prod. 2000, 60, 237–240.
106. Sinclair, M.; Zito, S.; Phillips, C. The Impact of Stakeholders’ Roles within the Livestock Industry on Their
Attitudes to Livestock Welfare in Southeast and East Asia. Animals 2017, 7, 6. [CrossRef] [PubMed]
107. Assurewel. Available online: http://www.assurewel.org/aboutassurewel (accessed on 22 August 2018).
108. FeatherWel. Available online: http://www.featherwel.org (accessed on 22 August 2018).
109. Mullan, S.; Szmaragd, C.; Cooper, M.; Wrathall, J.; Jamieson, J.; Bond, A.; Atkinson, C.; Main, D. Animal
welfare initiatives improve feather cover of cage-free laying hens in the UK. Anim. Welf. 2016, 25, 243–253.
[CrossRef]
110. Hennovation. Available online: http://hennovation.eu/index.html (accessed on 15 September 2018).
111. Van Dijk, L.; Buller, H.; MacAllister, L.; Main, D. Facilitating practice-led co-innovation for the improvement
in animal welfare. Outlook Agric. 2017, 46, 131–137. [CrossRef]
112. Van Staaveren, N.; Decina, C.; Baes, C.; Widowski, T.; Berke, O.; Harlander-Matauschek, A. A description of
laying hen husbandry and management practices in Canada. Animals 2018, 8, 114. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

29
 sustainability

Article
Social Sustainability Assessment of Canadian Egg
Production Facilities: Methods, Analysis,
and Recommendations
ID
Nathan Pelletier *
Natural Science and Engineering Research Council of Canada (NSERC)/Egg Farmers of Canada (EFC)
Industrial Research Chair in Sustainability, Department of Biology/Faculty of Management, University of
British Columbia Okanagan, Kelowna, BC V1V 1V7, Canada
* Correspondence: [email protected]; Tel.: +1-250-807-8245
Received: 19 March 2018; Accepted: 14 May 2018; Published: 16 May 2018

Abstract: A detailed assessment of the “gate-to-gate” social risks and benefits of Canadian egg
production facilities was undertaken based on the United Nations Environment Programme/Society
of Environmental Toxicology and Chemistry (UNEP/SETAC) Guidelines for Social Life Cycle
Assessment. Data were collected via survey from a representative subset of Canadian egg farms,
and evaluated against a novel suite of indicators and performance reference points developed for
relevance in the Canadian context. The evaluation focused on interactions with four stakeholder
groups (Workers; Local Communities; Value Chain Partners; and Society) in eighteen thematic areas.
This assessment resulted in a rich and highly nuanced characterization of the potential social risks
and benefits attributable to contemporary egg production facilities in Canada. Overall, risks were low
and benefits were identified for Local Communities, Value Chain Partners, and Society stakeholder
groups, but mixed for the Workers stakeholder group. With respect to the latter, identified areas of
higher risk are related, in particular, to a subset of indicators for Working Hours, Equal Opportunities
and Fair Salary. As such, the results suggest opportunities and strategies for the Canadian egg
industry both to capitalize on its current successes as well as to proactively engage in improving its
social sustainability profile. The study also contributes a novel set of social sustainability metrics
for use and continued development in the Canadian egg sector as well as other agri-food sectors in
Canada and beyond. The inevitable challenge in social life cycle assessment (LCA) of developing
non-arbitrary performance reference points for social indicators for which clear norms do not
exist, and similarly for establishing non-arbitrary scales and thresholds for differentiating between
performance levels, is underscored. A necessary next step with respect to the methods presented
herein is for stakeholder groups to carefully consider and refine the performance reference points
and characterization thresholds that have been developed, in order to assess their alignment with
context-specific social sustainability priorities for this industry, and also to extend the analysis to
encompass other value chain stages to enable a full social life cycle assessment.

Keywords: social life cycle assessment; social impact assessment methods; social sustainability;
eggs; Canada

1. Introduction
Social life cycle assessment (S-LCA) is the least developed of the three, complementary strands
of life cycle assessment, which provide analytical frameworks for life cycle-based sustainability
measurement and management [1]. In complement to environmental LCA and life cycle costing,
S-LCA is intended to improve decision support through understanding and identifying measures to
reduce the social impacts associated with product life cycles [2–5].

Sustainability 2018, 10, 1601; doi:10.3390/su10051601 30 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 1601

The “Guidelines for Social Life Cycle Assessment of Products” [6] provide the first major step
towards consensus methodologies for S-LCA. These guidelines provide “a map, a skeleton, and a
flashlight” [7] for implementation of S-LCA studies. In this context, “map” refers to the broad nature of
the guidelines and their preliminary nature. “Skeleton” reflects that the guidelines provide a foundation
on which it is envisaged that stakeholders will engage in fleshing out more specific methodological
requirements. “Flashlight” highlights that the guidelines illuminate future research needs [7]. In short,
considerable work remains—in particular with respect to developing widely accepted social indicators
and impact assessment methods, which may vary by sector/context. Uncertainty with respect to
scoring and weighting social sustainability performance for specific indicators remains a widely
recognized challenge [8]. Despite current limitations, the Guidelines are nonetheless the most widely
employed reference document for S-LCA studies [5,9,10].
Among published studies, researchers have developed and applied disparate indicators and
impact assessment methods. Variability in approach to indicator development and usage is reflected
in the range of qualitative through semi-quantitative and quantitative indicators that have been
employed [11–13]. With respect to impact assessment methods, the range of approaches may be in
part attributable to alternative paradigmatic bases for approaching S-LCA, as well as the necessity
of identifying context-appropriate reference points against which to assess social sustainability
performance [8,10,14,15]. The development of “Methodological Sheets of Subcategories of Impact for a
Social LCA” [16] has provided a first reference point for improving consistency in current practice.
Research has also varied in terms of bottom-up versus top-down approaches to social life cycle
assessment. Some authors have stressed the importance of context and company-specific assessments
(for example, see [17,18]), since social impacts may vary widely between companies producing
otherwise similar products. Others have emphasized the desirability of full supply chain social
life cycle inventory modelling and impact assessment, which is much more feasible when generic
social life cycle inventory data are employed [1]. In light of the general lack of detailed, process-level
social life cycle inventory databases to support full supply chain models in many contexts, gate-to-gate
studies are a common and necessary step to making such data available.
Use of social life cycle assessment in agri-food contexts has been limited to date, hence availability
of published case studies (for example, see [5,13–15,19]) is also limited. Among these, approaches to
indicator development and scoring are also varied—reflecting, in part, the highly diverse nature of
such contexts [8,13,15].
Eggs and egg products are an important part of the Canadian diet, and the egg industry makes a
significant contribution to national agricultural production in Canada [20]. Activities in this industry
have potential social risks and benefits for a wide range of stakeholders. To date, research efforts
have not been brought to bear in order to understand these potential risks and benefits in support of
improved decision making for social sustainability in this industry, nor have appropriate metrics for
assessing risks and benefits been advanced.
The general objective of the current analysis was to use the Guidelines for Social LCA [6] and
the Methodological Sheets of Subcategories of Impact for a Social LCA [16] as a basis for developing
and applying a suite of context-appropriate indicators and metrics to characterize the social risks
and benefits specific to activities at Canadian egg production facilities (i.e., what would be the egg
production stage in a full S-LCA of egg production). Taking the work of Reveret et al. [19] as inspiration,
the assessment used directly collected data from egg farmers in Canada to characterize social risks and
benefits for four stakeholder groups (Workers, Local Communities, Value Chain Partners, and Society).
Additional work will be necessary to similarly map social risks and benefits that may exist elsewhere
along egg value chains in support of a full social life cycle assessment of this industry.
The results of the study include a novel array of social indicators and performance reference points
appropriate to the Canadian egg farm context (but also adaptable for application in egg industries
elsewhere as well as other agri-food contexts), which should be further refined by egg industry
stakeholders looking forward. The results also include a first set of social science-based benchmarks of

31
Sustainability 2018, 10, 1601

the social benefits and risks attributable to Canadian egg production for the base year 2012. As such,
these results offer insights as to key leverage points for further improving the social sustainability
performance of egg production in Canada.
The format of the manuscript broadly mirrors the International Organization for Standardization
(ISO) 14044 norm in terms of the four stages of LCA, and the parallel UNEP/SETAC [6] guidelines for
social LCA. Section 2 (Methods) describes the Goal and Scope of the study, including details regarding
the collection of life cycle inventory (LCI) data, life cycle impact assessment (LCIA) categories and
methods, and objectives regarding the interpretation of the study. Section 3 provides detailed life cycle
impact assessment (LCIA) results, and Section 4 presents the interpretation and discussion of results.

2. Materials and Methods

2.1. Goal and Scope of the Study

This analysis was undertaken in order to develop and apply methods to characterize the
social risks and benefits for the stakeholder groups Workers, Local Communities, Value Chain
Partners, and Society associated with activities at contemporary Canadian egg facilities in 2012
(i.e., a “gate-to-gate analysis”). The goal was to arrive at a nuanced understanding of the current
social sustainability profile of egg facilities in Canada, supported by development of an appropriate
suite of social sustainability metrics, using data directly collected from industry participants and in
correspondence with the Guidelines for Social Life Cycle Assessment [6].
The system boundary for the assessment of Canadian egg production facilities is specific to the
activities of the participating facilities (i.e., a “gate-to-gate” analysis) and attendant interactions with
their stakeholders in 2012. The activity variable is 1000 egg facility worker hours (worker hours is
commonly used for this purpose in S-LCA), which results in 82.6 tonnes of egg production. Worker
hours was chosen because this will enable integration of future work examining other supply chain
stages, using this same aggregating activity variable, for a full social life cycle assessment. Moreover,
this will also allow expressing supply chain sustainability impacts per unit of eggs produced in parallel
to results from E-LCA studies. It is important to note here that, due to the focus on gate-to-gate
interactions only, it was not necessary to define aspects such as allocation principles, cut-offs, etc., nor
to develop a flow diagram.

2.1.1. Life Cycle Inventory Analysis

All data used for this detailed assessment of Canadian egg facilities were collected directly via
survey from industry participants. Supplementary Information A (SI A) presents the survey that was
used for data collection purposes. The survey was designed based on the stakeholder groups and
indicator categories described in the Guidelines for Social Life Cycle Assessment. Efforts were made to
ensure a representative sample, taking into account region of production (province-level) and farm
size. Surveys were administered by provincial egg boards and their field officers.

2.1.2. Life Cycle Impact Assessment Methods

According to the Guidelines for S-LCA, social life cycle impact assessment (S-LCIA) involves:

(a) aggregating some inventory data within subcategories and categories; and
(b) making use of additional information, such as internationally accepted levels of minimum
performance, to help understand the magnitude and the significance of the data collected in the
Inventory phase.

However, in contrast to environmental life cycle impact assessment, standardized, widely accepted
social life cycle impact assessment methods that allow aggregation of different kinds of social risk are
not yet available for social life cycle assessment. The Guidelines do, however, refer to Methodological

32
Sustainability 2018, 10, 1601

Sheets of Subcategories of Impact for a Social LCA [16], which were consulted in order to identify
relevant sub-categories for the current analysis.
The S-LCIA stage of this facility-specific analysis focuses on interpretation and presentation of
the social life cycle inventory data that were collected from Canadian egg facilities and associated
impact assessment results, with results organized by stakeholder group and social theme following the
Guideline recommendations. Four stakeholder groups were considered: Workers; Local Communities;
Value Chain Partners; and Society (Consumers were not considered, since the analysis did not extend
beyond the egg facility gate). Data and results were further organized within each stakeholder group
into subcategories. Table 1 describes the stakeholder groups and subcategory combinations that
were evaluated.

Table 1. Stakeholder groups, social themes considered in the social life cycle assessment of Canadian
egg facilities.

STAKEHOLDER: WORKERS
Freedom of association and collective bargaining rights
Fair salary
Working hours
Equal opportunities
Health and safety
Social benefits, social security, and job security
STAKEHOLDER: LOCAL COMMUNITY
Access to resources
Safe and healthy living conditions
Respect for indigenous rights
Community engagement
Local employment
STAKEHOLDER: SOCIETY
Public commitment to sustainability issues
Contribution to economic development
Employee training
Corruption
STAKEHOLDER: VALUE CHAIN PARTNERS
Fair competition
Promoting social responsibility
Supplier relationships

Establishing Performance Reference Points

In order to interpret the social sustainability performance of Canadian egg production facilities,
it was necessary to identify performance reference points (PRPs) for either ideal or minimum acceptable
performance along a spectrum of possible performance levels for the subcategory indicators for
each social theme. These reference points were chosen, to the extent possible, relative to relevant
international and/or Canadian norms. In many cases, however, clear norms were not identifiable as a
basis for assessing performance. In such cases, thresholds for differentiating between performance
levels were instead based either on ideal performance (for example, a zero percent incidence rate of
an undesirable outcome, or a one hundred percent incidence rate of a desirable outcome) or based
on % incidence rate along a continuum from undesirable to desirable outcomes. In some cases,
more than one norm was identified as potentially relevant. Here, results are presented for each norm.
Supplementary Information B (SI B) provides a series of 17 tables describing impact subcategories and
subcategory indicators, and reporting the performance reference points and thresholds used to assess
performance for each indicator.
It is important to note here that, where clear norms do not exist, the determination of
performance reference points is subjective and somewhat arbitrary. Ideally, these should be defined
in stakeholder-specific contexts via deliberative democratic procedures that reflect a shared value
structure and objectives. For example, within the egg industry, stakeholders could potentially engage

33
Sustainability 2018, 10, 1601

in dialogue and processes aimed at determining thresholds that correspond with shared industry
values and objectives regarding social sustainability outcomes. For the purpose of the current analysis,
many of the performance reference points were researcher-defined and should hence be viewed as
placeholder values only. They might also be viewed, however, as a basis for benchmarking, tracking
changes, and goal setting with respect to the sustainability performance of the industry over time
relative to the 2012 benchmark results.
To assist in the presentation of performance levels, the S-LCIA results are colour coded so as
to indicate the performance levels achieved by the industry in 2012. The system of color codes
developed by Reveret et al. [19] to represent performance levels for a social life cycle assessment of
the Canadian dairy industry is adopted. This system utilizes a scale spanning four performance
levels (Figure 1). These are “risky behaviour,” “compliant behaviour,” “proactive behaviour,”
and “committed behaviour”.
A risky behaviour is a practice that may potentially result in a serious, undesirable consequence
for stakeholders. This includes illegal behaviours as well as behaviours that, although not illegal,
may generally be viewed as negative.
A compliant behaviour is one that meets minimum requirements, norms or expectations.
This performance level signifies that the organization is not acting in a risky manner, nor is it making
any proactive efforts to achieve a socially desirable outcome.
A proactive behaviour is one that indicates some level of initiative towards achieving a more
socially desirable outcome than may be legally required.
A committed behaviour is one that reflects leadership or clear striving to achieve socially
desirable outcomes. This level of behaviour goes beyond marginal improvements by demonstrating
considerably better outcomes than would be associated with compliant behaviour.

Figure 1. Colour codes employed to characterize performance levels relative to performance

reference points.

Performance levels were assigned based on specific thresholds for each indicator as described
in SI B. A fixed scale for thresholds was not feasible—rather, thresholds deemed appropriate to
differentiating performance levels for each indicator were developed. As with the assignment of PRPs
in the absence of clear norms, the assignment of threshold levels is inevitably somewhat arbitrary
unless defined in stakeholder-specific contexts via deliberative democratic procedures that reflect a
shared value structure and objectives. This is a widely recognized challenge in S-LCA [6,16].
The methodology for defining the performance reference points and thresholds for each
stakeholder group/social theme/sub-category indicator are schematically described in Figure 2.
Detailed descriptions of the category indicator-specific methods and rationales are provided in SI B
(Tables S1–S17).

Figure 2. Schematic representation of the relationships between performance reference

points/thresholds for each stakeholder group/social theme/sub-category indicator combination
utilized in the social life cycle impact assessment.

34
Sustainability 2018, 10, 1601

It should also be noted that not all performance levels are relevant for all indicators. For example,
if no clear norm for an indicator can be identified, then a “risky” behavior cannot be assessed.
Nonetheless, it is still useful (for example, for the purpose of benchmarking or sectoral goal setting)
to differentiate between the performance of companies, which may engage in socially desirable
behaviours to varying degrees, despite the lack of any clear norm or requirement.
To facilitate an accessible presentation of results in Figures 3–7, in some cases, indicator results are
aggregated if the same performance score/colour code is assigned for multiple related indicators for a
subcategory that can be expressed under a common indicator heading. Aggregation and weighting
are not otherwise applied.

2.1.3. Interpretation and Recommendations

The Life Cycle Interpretation phase requires systematically reviewing the results of the Life Cycle
Impact Assessment phase with respect to the research questions. Here, the interpretation phase focuses
in particular on:

• elucidating the key social risks and benefits for stakeholders that are specifically associated with
activities that occur at Canadian egg production facilities.
• identifying priority areas for interventions to improve the social license of Canadian egg
producers, either via communications regarding the social benefits associated with the egg
industry, or commitments to monitor and seek to improve the social sustainability profile of
Canadian egg production with respect to specific social risk areas.
• identifying priority areas for further data collection and research.
• highlighting weaknesses of the current study and recommending areas for further research and
methods development.

3. Results

3.1. Life Cycle Inventory Results

In total, usable surveys were collected from 59 egg facilities together representing 357,286 worker
hours in Canada in 2012. The number of part- and full-time workers employed in these facilities was
248, with an average of 1440.7 h worked per worker per year. For detailed social life cycle inventory
results for each indicator, see SI C Tables S18–S35, which present the social life cycle inventory
data, expressed as worker hour-weighted average results, as well as low and high reported values
where relevant.

3.2. Life Cycle Impact Assessment Results

Figures 3–7 present summary social life cycle impact assessment results for each stakeholder
group, social theme and sub-category indicator. For detailed social life cycle impact assessment results
for each sub-category indicator, please see SI D Tables S36–S53.

STAKEHOLDER: WORKERS
Figures 3 and 4 provide a summary of LCIA results for the Workers stakeholder category.

Freedom of Association and Collective Bargaining Rights

No employers indicated that employment at their facilities is conditioned by any restrictions on
the right of employees to collective bargaining (compliant). However, for only 28% of worker hours
did respondents indicate that employees are free to join unions of their choice. Moreover, a 0% union
representation rate was reported and it would also appear that participation of employees in
organizational planning is not currently the industry norm. Only for 10% of worker hours was
it indicated that employees have access to neutral, third-party dispute resolution. Based on the current

35
Sustainability 2018, 10, 1601

Canadian average rate of union representation a risky behaviour is assessed. In light of current lack
of norms but low levels of provision, compliant behaviours are assessed with respect to employee
participation, codified minimum notice periods regarding operational changes, and employee access to
neutral, binding, and independent dispute resolution procedures. The Canadian egg industry might,
however, consider options for improving employee representation and participation (SI D Table S36).

Fair Salary
Minimum wage standards were exceeded across the Canadian egg facilities surveyed for both the
lowest paid and average employee, hence, on this basis, a “proactive” score is assigned. The majority
(77%) of workers receive at least 10% more than the minimum wage, 41% earn at least 50% more,
and 26% earn at least 100% more than the minimum wage. Relative to norms for Canadian agricultural
workers, wages for the lowest paid employees at some Canadian egg facilities might be considered
risky in that they are below this average. Average employee wages are, however, similar to the average
for Canadian agricultural workers and hence a compliant score is assessed for this indicator.
Another area for improvement is with respect to the regularity and documentation of pay. For only
57% of worker hours did respondents indicate that regular documentation of pay was provided. Here,
a risky behaviour is assessed. There were no reported complaints regarding deductions on wages,
hence a compliant behaviour is assessed for this indicator (SI D Table S37).

Figure 3. Social life cycle impact assessment scores for Canadian egg facilities in 2012 with respect to
the stakeholder group “Employees” (freedom of association and collective bargaining rights, fair salary,
working hours).

36
Sustainability 2018, 10, 1601

Figure 4. Social life cycle impact assessment scores for Canadian egg facilities in 2012 with respect to the
stakeholder group “Employees” (equal opportunities, health and safety, social benefits, social security
and job security).

Working Hours
The weighted average work week for employees in Canadian egg facilities in 2012 was 38.83 h,
which is slightly higher than the Canadian average but much lower than the ILO maximum of 48 h
(compliant behaviour). This is, however, likely consistent with working hours elsewhere in the
agricultural sector. The longest average work week is 47 h (compliant behaviour). Respondents also
indicated, however, that more than 10% of working hours correspond to work weeks in excess of
48 h. Here, a risky behaviour is assessed. There is also a very low incidence of contractual agreements
regarding working hours and overtime compensation (risky behavior).
Although some employers report paying their employees a 50% overtime premium, overall,
the survey data indicate a low rate of overtime pay (5.8% on average) in Canadian egg facilities.
This seemingly corresponds to the norm for the Canadian agriculture sector (compliant behaviour).
However, if the norm for Canadian workers as a whole is taken as the reference point, then a risky
behaviour is assessed (SI D Table S38).

Equal Opportunities
Based on reported data, employees on Canadian egg farms are largely Caucasian (97%) and male
(63%), with an even age class distribution. Twenty-eight percent of respondents reported having a
formal equal opportunities policy in place for their facilities (proactive behaviour). In many cases,
lack of such a policy may simply reflect that the facilities are small family/owner operated facilities

37
Sustainability 2018, 10, 1601

with no other employees. However, if equality of representation of males and females is taken as the
performance reference point (compliant behaviour), or a proportionate degree of inclusion of visible
minorities (risky behaviour), then there may, indeed, be space for improvement in this regard. This is
similarly true for representation of females and visible minorities in management positions (risky
behaviour).
Considering salary equality, it would appear that male and female employees receive equal
remuneration (compliant behaviour). However, female managers apparently receive lower salaries
(85%) relative to male managers (risky behaviour) (SI D Table S39).

Health and Safety

According to Employment and Social Development Canada (ESDC) [21], in Canada “one in every
68 employed workers in 2010 was injured or harmed on the job and received workers compensation as
a result”. Although 2.7 works days were lost, on average, due to occupational accidents, injuries or
illness in Canadian egg production facilities, only 0.14 WCB claims were filed per facility industry-wide,
which is well below the Canadian average. No medically-diagnosed, work-related diseases or fatalities
were reported (compliant behaviour).
Respondents indicated that 53% of worker hours occurred in workplaces characterized by high
levels of noise, fumes, or dust (risky behaviour). While all employees are provided with appropriate
protective gear when required to handle hazardous materials (committed), only half are reportedly
trained in handling such materials (proactive).
Employees generally have access to clean water and sanitary facilities (compliant behavior) and,
in most cases (82% of worker hours—committed behaviour) first aid equipment is maintained and
available to employees. A trained, designated first aid attendant was available for 62% of the reported
worker hours (proactive behaviour). A dedicated Health and Safety plan is in place for 45% of the
worker hours (proactive behavior), and a dedicated Health and Safety manager for 31% of the worker
hours (proactive behaviour).
Overall, it would appear that health and safety incidents were low in 2012, but that the Canadian
egg industry would benefit from development and implementation of industry-wide standards with
respect to health and safety plans, management, and training. The average surveyed Canadian egg
facility invested $1762 in health and safety measures in 2012 (SI D Table S40).

Social Benefits, Social Security, and Job Security

It would appear that the provision of social benefits is not consistent within the Canadian egg
industry. Health insurance benefits are provided to less than half of employees, dental and retirement
benefits to roughly one third, and child care and/or maternity/paternity benefits to less than one
employee in seven. Across these five categories, the average social benefit provision level is 30%.
It should be noted here that some employers in Canadian egg facilities do offer full social benefits to
their employees, while others offer none.
With respect to employment contracts, only 1/4 of worker hours were subject to formal
employment contracts in 2012. Of these, roughly 2/3 were full time contracts, and 1/3 were part
time contracts. The majority of reported worker hours were not subject to an employment contract.
This indicates a low level of job security. Based on a reference level of a 100% formal contract rate,
a risky behavior is assessed.
According to the Conference Board of Canada (CBC) [22], the voluntary employee turn-over rate
in Canada in 2012–2013 was 7.3%, and the involuntary turn-over rate was 3.7%. Employee turn-over
rates in Canadian egg facilities were comparatively low (4.1% overall). Half of employees who left jobs
at Canadian egg facilities in 2012 quit, while one quarter were dismissed. Compared to the Canadian
average, a compliant behaviour is assessed (SI D Table S41).

38
Sustainability 2018, 10, 1601

STAKEHOLDER: LOCAL COMMUNITY

Figure 5 provides a summary of LCIA results for the Local Community stakeholder category.

Access to Resources
The total expenditures of egg facilities on infrastructure with mutual community access and
benefit in 2012 were very low (compliant behaviour assessed). However, some survey respondents
spent as much as $26,000 on voluntary, charitable donations and investments in their community,
with an average of $2205 per facility (proactive behaviour assessed) (SI D Table S42).

Safe and Healthy Living Conditions

Only one accident in a local community was reported across surveyed facilities for 2012, hence the
industry average accident rate is very low. This single accident is taken as an outlier, hence a
compliant score is assigned. However, while many facilities did not receive any complaints from
the local community regarding nuisance issues, some facilities received as many as two complaints.
Overall, 0.4 complaints were received per facility in 2012. Relative to an ideal scenario performance
reference point of 0 complaints, a risky behaviour is assessed.
In light of the complaint rate, it would seem prudent to having in place formal protocols to
maintain living conditions, minimize risk, and respond to grievances in the community. Twenty-seven
percent of facilities reported having formal protocols in place to maintain safe and healthy living
conditions, while 32% have formal protocols to minimize risk and 17% have formal protocols to
respond to grievances (proactive behavior). No fines for infringements at the local level were reported
(compliant behavior).
One current approach to ensuring safe and healthy living conditions in local communities and
minimizing risk is the implementation of an environmental farm management plan. Two thirds
of worker hours occurred at facilities having an environmental farm management plan in 2012.
Here, proactive behavior is assessed (SI D Table S43).

Respect for Indigenous Rights

While the survey data indicate that no complaints were received by Canadian egg facilities from
First Nations community members in 2012, it is notable that no meetings were held with First Nations
members. Also notable is that only 2% of worker hours were reported to occur in areas where land
rights conflicts exist (risky behavior), which is unlikely to be accurate, and that only 2% of worker hours
occurred in facilities having formal policies in place to protect the rights of indigenous community
members. As no norms exist in this regard, compliant behaviors are assessed. It is nonetheless
recommended that proactive behavior be encouraged in this domain (SI D Table S44).

Community Engagement
Only 7% percent of worker hours in 2012 occurred in egg facilities having formal policies
on community engagement in place (compliant behavior). Reported attendance of meetings with
stakeholder groups was variable, with some facilities reporting having attended as many as six
meetings. On average, reporting facilities devoted 9 volunteer hours to community initiatives in 2012.
Here, proactive behaviours are assessed (SI D Table S45).

Local Employment
Although less than 1/3 of Canadian egg facilities report having a formal policy regarding
local hiring (proactive behavior), the local hiring rate was 87% in 2010 (committed behavior).
Similarly, the majority share (64%) of goods and services purchased by egg facilities was locally
sourced (proactive behavior) (SI D Table S46).

39
Sustainability 2018, 10, 1601

Figure 5. Social life cycle impact assessment scores for Canadian egg facilities in 2012 with respect to
the stakeholder group “Local Community”.

STAKEHOLDER: VALUE CHAIN PARTNERS

Figure 6 provides a summary of LCIA results for the Value Chain Partners stakeholder category.

Fair Competition
Although no facilities reported having documentation of procedures to prevent engaging in or
being complicit in anti-competitive behaviours (compliant), no legal actions, fines or complaints were
reported for 2012 (compliant) (SI D Table S47).

Promoting Social Responsibility

Three percent of worker hours occurred in facilities that report adhering to a specific code of
conduct regarding the protection of human rights (compliant behavior). No supplier audits for
environmental or social responsibility were reported (compliant behavior). Canadian egg facilities
surveyed for this study participated in a weighted average of 0.16 initiatives to promote value chain
environmental or social responsibility, with a range from 0 to 5 initiatives per facility (proactive
behavior). In light of this low activity level, it would seem that there is opportunity here for initiatives
to enhance the promotion of social responsibility in the Canadian egg industry (SI D Table S48).

40
Sustainability 2018, 10, 1601

Supplier Relationships
Overall, it appears that Canadian egg facilities maintain good relationships with their value chain
partners. No complaints were received from suppliers with respect to coercive communications or
insufficient lead time in 2012, and a weighted average of 0.01 complaints were received (representing
one facility with two complaints, which is taken as an outlier) with respect to timeliness of payments.
On the basis of this very low level, a compliant behavior is assessed for the industry as a whole (SI D
Table S49).

STAKEHOLDER: SOCIETY
Figure 7 provides a summary of LCIA results for the Society stakeholder category.

Figure 6. Social life cycle impact assessment scores for Canadian egg facilities in 2012 with respect to
the stakeholder group “value chain partners”.

41
Sustainability 2018, 10, 1601

Figure 7. Social life cycle impact assessment scores for Canadian egg facilities in 2012 with respect to
the stakeholder group “Society”.

Public Commitment to Sustainability

Among those surveyed, only 8% of worker hours occurred in facilities having publicly available
CSR or other documents that communicate commitments to sustainability issues (compliant behaviour).
For 1%, specific mechanisms are in place to ensure the realization of such commitments (compliant
behaviour). On this basis, it would appear that documentation and communication of sustainability
commitments is not currently widespread in the Canadian egg industry.
Outside of formal commitments and communications, however, some egg facilities are, indeed,
engaging in sustainability initiatives. Facilities report an average of over 10 h devoted to sustainability
programs in 2012 (committed behavior). Some facilities were active members in programs to support
sustainable business practices (proactive behavior), and others received awards for engagement in
sustainability issues (proactive behavior). The average expenditure on sustainability programs was
$803 (proactive behavior). No complaints were reported with respect to non-fulfillment of sustainability
commitments or activities to undermine sustainability measures (compliant behaviour).
In sum, it would appear that monitoring and communicating with respect to sustainability issues
is not currently the norm in the Canadian egg industry, but that some facilities are already actively
engaged in this domain. A significant opportunity may hence exist to enhance the social license
of Canadian egg facilities through implementation and documentation of formalized sustainability
commitments (SI D Table S50).

42
Sustainability 2018, 10, 1601

Contribution to Economic Development

The scale of these contributions varies widely between egg facilities, reflecting the commensurately
broad range in size of operations. For example, total revenue ranges from $260,000 to $9,464,000,
with an industry average of $2,508,000 among reporting facilities. On average, participating Canadian
egg facilities paid $248,000 of wages in 2012, along with $78,000 in taxes and reported an average of
$1,758,000 in total expenses (SI D Table S51).

Employee Training
Significant resources were dedicated to employee training in Canadian egg facilities in 2012.
On average, workers were provided with 53 h of training in 2012 (committed behaviour), and total
expenses related to employee training averaged $529 per facility (proactive behaviour) (SI D Table S52).

Corruption
Two convictions for violations of corruption-related laws or regulations were reported by a single
facility, with an accompanying fine of $500. This single facility report is therefore taken as an outlier, as
it would appear that such violations are not commonplace within the Canadian egg industry (hence
compliant scores are assigned) (SI D Table S53).

4. Discussion
The results of this assessment provide a rich and highly nuanced characterization of the potential
social risks and benefits attributable to contemporary egg production facilities in Canada. They provide
a series of first benchmarks for the Canadian egg industry. They also highlight where and to what extent
stakeholders are currently benefiting from positive social contributions made by the industry—for
example, through local job creation, high levels of employee training, provision of protective gear and
first aid equipment for employees, and time devoted to sustainability programs (areas where facilities
demonstrated “committed” behaviors). These contributions go beyond what is otherwise required by
law. The results also point towards areas of potential social risk for some stakeholders (such as the
low incidence of formal employment contracts and union representation for workers, low levels of
overtime compensation, or sub-optimal workplace diversity and equality). As such, the results suggest
opportunities and strategies for the Canadian egg industry both to capitalize on its current successes
as well as to proactively engage in improving its social sustainability profile.
For the “Workers” stakeholder category, the directly collected data confirmed the very low level
of representation and collective bargaining for employees of egg facilities. The representation rate
of 0% was much lower than the Canadian average of 31%, but likely in-line with current norms for
the Canadian agricultural sector. Similarly, employee salaries appear to be consistent with Canadian
agricultural worker norms, but lower than those of the average Canadian. Most employees are,
in fact, remunerated at levels significantly higher than the minimum wage, but a small fraction of
employees receive full- or part-time minimum wage salaries. Province-by-province assessments of
employee wages relative to regional living wage estimates are recommended in order to ensure that
the lowest paid employees are not at risk. Compensation for overtime pay should also be monitored,
and industry-wide norms developed. On average, worker hours are within acceptable norms although
a small fraction of employees work in access of 48 hours per week. Overall, improvements with respect
to formal, contractual agreements for employees regarding working conditions are recommended.
With respect to equal opportunities in the Canadian egg facility workplace, the majority of
employees are currently Caucasian males. Visible minorities have a very low level of representation in
this workforce. For general employees, salaries are equitable for males and females. However, the data
collected for 2012 suggest a disparity in pay for female compared to male managers of roughly 15%.
Additional research and possible mitigation strategies may be desirable to increase diversity and
ensure equality for employees.

43
Sustainability 2018, 10, 1601

Health and safety conditions for workers in Canadian egg facilities appear to be very good.
Although facilities are often characterized by high levels of dust and/or noise, employers report high
levels of worker training, use of protective gear, and access to first aid equipment and sanitary facilities.
Many facilities report the use of dedicated health and safety plans, as well as designated first aid
attendants. No medically-diagnosed, workplace-related diseases or fatalities were reported for 2012.
Provision of social benefits to workers varies widely between egg facilities. Many facilities report
providing at least one non-mandatory social benefit and some more than three. Others provide no
additional benefits to employees. This suggests opportunities for the development of norms within
the Canadian egg industry to promote consistent provision of non-mandatory social benefits in order
to improve conditions for employees. Improving job security through the implementation of formal
employment contracts is also recommended, as current usage of contractual agreements is low.
For the stakeholder group “Local Community,” it would appear that Canadian egg facilities
are often proactively engaged in making meaningful contributions to the communities in which
they operate. Egg facilities largely employ local community members, and source a large fraction of
inputs from local businesses. Most facilities reported some level of voluntary, charitable donations
or investments in their communities, with an average of $2205 spent on local community initiatives
per facility in 2012. Participation in community initiatives is also high. In addition, many facilities
report implementation of an Environmental Farm Management Plan, which serves to reduce risk of
nuisance issues, as well as the existence of formal protocols to mitigate risk for local communities
and respond to grievances. The overall accident rate in local communities as a result of egg facility
activities was very low. One area of potential social risk relates to interactions with indigenous
communities. Although many egg facilities are situated in communities proximate to First Nations
communities, only 2% reported operating in areas where land rights conflicts exist, and reported levels
of proactive engagement with First Nations communities were low. Formalizing “good neighbour”
policies and outreach may be desirable. This could potentially be paired with initiatives to increase
workplace diversity.
Management decisions and activities similarly impact on society at large, and may result
in either societal risks or benefits. Demonstrating commitment to and actions consistent with
contributing positively to society is fundamental to the concept of corporate social responsibility
(CSR). CSR reporting, including transparent mechanisms for measuring, monitoring, goal setting
and follow-up, is increasingly important to maintaining social license, as well as accessing emerging
market opportunities associated with sustainability objectives.
Many Canadian egg facilities are already taking steps to improve and promote the sustainability
of their practices. Facilities reported an average of 10 h devoted to sustainability initiatives in 2012,
and related expenses of roughly $800 per facility. Development and reporting of formal CSR documents
is, however, relatively uncommon. An industry-wide initiative to support operators in developing and
implementing CSR strategies is strongly encouraged. Indeed, in light of increased attention by both
commodity groups and large retailers to developing and implementing sustainability measurement,
reporting and certification requirements, it is strongly recommended that the Canadian egg industry
become proactive in this respect. This will require the support and cooperation of both producers and
their representative bodies in order to develop and implement industry-wide strategies and initiatives.
Social life cycle assessment is a relatively new field of research, and methodological development
is on-going. To date, very few social LCA studies of food products have been reported (for example,
see [11,13,14,19,23,24]). Varied approaches have often been employed [11,12] and, given the diversity
of agri-food production contexts, the feasibility and desirability of consistency between studies
is debatable.
The current analysis represents only a partial (i.e., gate-to-gate) evaluation of the potential social
risks and benefits attributable to the Canadian egg industry. Future work should expand the analysis
to encompass value chain stages and stakeholder interactions both upstream and downstream of
Canadian egg facilities. While considerable efforts were invested to ensure appropriate representation

44
Sustainability 2018, 10, 1601

across regions of production (provinces) and farm size, the sample nonetheless represents a relatively
small subset of egg production facilities in Canada. In this respect, “scaling up” results is challenging,
and collecting larger data samples wherever feasible in such analyses is clearly desirable. The survey
questions (and related indicators that can be assessed) should also be periodically revisited so as to
ensure that all relevant social sustainability issues are taken into consideration—in particular given
that conditions may change over time, and the suite of social sustainability issues deemed appropriate
for inclusion in such analyses will likely continue to evolve. Moreover, while the impact assessment
methods that were developed here provide a valuable example of how social risks and benefits might
be assessed in egg production or for other food production activities, it is important to note that
defining performance reference points for social life cycle impact assessment where clear norms do not
exist is challenging and inevitably somewhat arbitrary. This is similarly true with respect to identifying
appropriate thresholds for distinguishing between levels of “sustainability performance” for each
indicator considered, even where norms do exist. Multiple, competing bases are possible. For this
reason, it is essential that methods and data are transparently presented so as to enable identification
of potential real or perceived bias. Moreover, it may be preferable to present results at the indicator
level (as in the current study) rather than aggregating results across indicators, since such aggregation
requires weighting (introducing an additional level of uncertainty and potential bias) and may also
bias interpretation if numerous “easy to achieve” norms outweigh a limited number of more important
social sustainability performance indicators.
Clearly, a desirable next step, in the extension of this methods development and analysis
exercise, is for the Canadian egg industry to engage in a multi-stakeholder dialogue in order to
define mutually agreed upon, clear thresholds for performance levels as well as goals for social
sustainability performance in this industry [13]. The novel set of social sustainability metrics developed
here can therefore provide a useful starting point for continued development and application in the
Canadian egg sector and may be usefully adapted for application in other agri-food sectors in Canada
and beyond.

Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/5/

1601/s1, SI A—Social Life Cycle Inventory Survey, SI B—Social Life Cycle Impact Assessment Indicators and
Performance Reference Points, SI C—Detailed Social Life Cycle Inventory Results, and SI D—Detailed Social Life
Cycle Impact Assessment Results.
Funding: This research was funded by Egg Farmers of Canada. Publication was supported through the
NSERC/Egg Farmers of Canada Industrial Research Chair in Sustainability.
Conflicts of Interest: The author declares no conflict of interest. The funding sponsors had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the
decision to publish the results.

References
1. Pelletier, N.; Sala, S.; Ostaglu, E.; Rosenbaum, E.; Vasta, A.; Benoit-Norris, C.; Norris, G. Social sustainability
in trade and development policy. Int. J. Life Cycle Assess. 2018, 23, 629–639. [CrossRef]
2. Jorgensen, A.; Le Bocq, A.; Nazarkina, L.; Hauschild, M. Methodologies for social life cycle assessment. Int. J.
Life Cycle Assess. 2008, 13, 96–103. [CrossRef]
3. Jorgensen, A.; Lai, L.; Hauschild, M. Assessing the validity of impact pathways for child labour and wellbeing
in social life cycle assessment. Int. J. Life Cycle Assess. 2010, 15, 5–16. [CrossRef]
4. Jorgensen, A. Social LCA—A way ahead? Int. J. Life Cycle Assess. 2013, 18, 296–299. [CrossRef]
5. Zamagni, A.; Feschet, P.; De Luca, A.; Iofrida, N.; Buttol, P. Social Life Cycle Assessment: Methodologies
and Practice. In Sustainability Assessment of Renewables-Based Products: Methods and Case Studies; Dewulf, J.,
De Meester, S., Rodrigo, A., Eds.; Wiley: New York, NY, USA, 2015; Available online: http://ca.wiley.com/
WileyCDA/WileyTitle/productCd-111893394X.html# (accessed on 5 January 2017).
6. UNEP/SETAC. Guidelines for Social Life Cycle Assessment of Products. In The UNEP/SETAC Life Cycle
Initiative; UNEP/SETAC: Paris, France, 2009.

45
Sustainability 2018, 10, 1601

7. Benoit-Norris, C.; Norris, G.; Valdivia, S.; Ciroth, A.; Moberg, A.; Bos, U.; Prakash, S.; Ugaya, C.; Beck, T.
The guidelines for social life cycle assessment of products: Just in time! Int. J. Life Cycle Assess. 2010, 15,
156–163. [CrossRef]
8. Do Carmo, B.; Margni, M.; Baptiste, P. Addressing uncertain scoring and weighting factors in social life cycle
assessment. Int. J. Life Cycle Assess. 2017, 22, 1609–1617. [CrossRef]
9. Wu, R.; Yang, D.; Chen, J. Social life cycle assessment revisited. Sustainability 2014, 6, 4200–4226. [CrossRef]
10. Iofrida, N.; De Luca, A.; Strano, A.; Gulisano, G. Can social research paradigms justify the diversity of
approaches to social life cycle assessment? Int. J. Life Cycle Assess. 2018, 23, 464–480. [CrossRef]
11. Paragahawewa, U.; Blackett, P.; Small, B. Social Life Cycle Analysis (S-LCA): Some Methodological Issues and
Potential Application to Cheese Production in New Zealand; AgResearch Ltd.: Palmerston North, New Zealand,
2009.
12. Smith, J.; Barling, D. Social impact and life cycle assessment: Proposals for methodological development for
SMEs in the European food and drink sector. Int. J. Life Cycle Assess. 2014, 19, 944–949. [CrossRef]
13. De Luca, A.; Iofrida, N.; Strano, A.; Falcone, G. Social life cycle assessment and participatory approaches:
A methodological proposal applied to citrus farming in Southern Italy. Integr. Environ. Assess. 2015, 11,
383–396. [CrossRef] [PubMed]
14. Chen, W.; Holden, N. Social life cycle assessment of average Irish dairy farm. Int. J. Life Cycle Assess. 2017,
22, 1459–1472. [CrossRef]
15. Petti, L.; Ramirex, P.; Traverso, M.; Ugaya, C. An Italian tomato “Cuore di Bue” case study: Challenges and
benefits of using subcategory assessment method for social life cycle assessment. Int. J. Life Cycle Assess.
2018, 23, 569–580. [CrossRef]
16. Benoît-Norris, C.; Vickery-Niederman, G.; Valdivia, S.; Franze, J.; Traverso, M.; Ciroth, A.; Mazijn, B.
Introducing the UNEP/SETAC methodological sheets for subcategories of social LCA. Int. J. Life Cycle Assess.
2011, 16, 682–690. [CrossRef]
17. Spillemaecker, S.; Vanhoutte, G.; Traverniers, L.; Lavrysen, L.; van Braeckel, D.; Mazijin, B.; Rivera, J.
Integrated Product Assessment: The Development of the Label ‘Sustainable Development’ For Products, Ecological,
Social, and Economical Aspects of Integrated Product Policy; Belgian Science Policy: Brussels, Belgium, 2004.
18. Dreyer, L.; Hauschild, M.; Schierbeck, J. Characterisation of social impacts in LCA. Int. J. Life Cycle Assess.
2010, 15, 247–259. [CrossRef]
19. Reveret, J.P.; Couture, J.M.; Parent, P. Socio-economic LCA of milk production in Canada. In Social Life Cycle
Assessment; Muthu, S., Ed.; Springer Science + Business Media: Singapore, 2015. [CrossRef]
20. AAFC. Canada’s Poultry and Egg Industry Profile at a Glance; Agriculture and Agri-Food Canada: Ottawa, ON,
Canada, 2013.
21. ESDC. Work—Work-Related Injuries. Indicators of Well-Being in Canada; Employment and Social Development
Canada: Toronto, Canada, 2015. Available online: http://www4.hrsdc.gc.ca/[email protected]?iid=20
(accessed on 10 June 2016).
22. CBC. What Are the Overall Voluntary and Involuntary Turnover Rates for Canadian Organizations? HR Questions
and Answers; Conference Board of Canada: Ottawa, ON, Canada, 2015; Available online: http://www.
conferenceboard.ca/topics/humanresource/questions.aspx#Q1 (accessed on 10 June 2016).
23. Kruse, S.; Flysjo, A.; Kasperczyk, N.; Scholz, A. Socioeconomic indicators as a complement to life cycle
assessment—An application to salmon production systems. Int. J. Life Cycle Assess. 2009, 14, 8–18. [CrossRef]
24. Manik, Y.; Leahy, J.; Halog, A. Social life cycle assessment of palm oil biodiesel: A case study in Jambi
Province of Indonesia. Int. J. Life Cycle Assess. 2013, 18, 1386–1392. [CrossRef]

© 2018 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

46
 sustainability

Article
Study on the Vertical Linkage of Greenhouse Gas
Emission Intensity Change of the Animal Husbandry
Sector between China and Its Provinces
Tianyi Cai 1,2 , Degang Yang 1, * ID
, Xinhuan Zhang 1 , Fuqiang Xia 1 and Rongwei Wu 1,2 ID

1 Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China;
[email protected] (T.C.); [email protected] (X.Z.); [email protected] (F.X.);
[email protected] (R.W.)
2 University of Chinese Academy of Sciences, Beijing 100049, China
* Correspondence: [email protected]; Tel.: +86-0991-7827319

Received: 30 May 2018; Accepted: 13 July 2018; Published: 16 July 2018

Abstract: China’s carbon intensity (CI) reduction target in 2030 needs to be allocated to each province
in order to be achieved. Thus, it is of great significance to study the vertical linkage of CI change
between China and its provinces. The existing research on the vertical linkage focuses more on
energy-related economic sectors in China; however, attention has not been paid to China’s animal
husbandry (AH) sector, although the role of the China’s AH sector in greenhouse gas (GHG) reduction
is increasingly important. This study firstly established a vertical linkage of change in greenhouse
gas emission intensity of the animal husbandry sector (AHGI) between China and its 31 provinces
based on the logarithmic mean Divisia index (LMDI) decomposing method from the perspective
of combining emission reduction with economic development, and quantified the contributions of
each province and its three driving factors of environmental efficiency (AHEE), productive efficiency
(AHPE), and economic share (AHES) to reducing China’s AHGI during the period of 1997–2016.
The main results are: (1) The AHGI of China decreased from 5.49 tCO2 eq/104 yuan in 1997 to
2.59 tCO2 eq/104 in 2016, showing a 75.25% reduction. The AHGI in 31 provinces also declined
and played a positive role in promoting the reduction of national AHGI, but there were significant
inter-provincial differences in the extent of the contribution. Overall, the provinces with higher
emission levels contributed the most to the reduction of China’s AHGI; (2) The AHPE and AHEE
factors in 31 provinces cumulatively contributed to the respective 68.17% and 11.78% reduction of
China’s AHGI, while the AHES factors of 31 provinces cumulatively inhibited the 4.70% reduction.
Overall, the AHPE factor was the main driving factor contributing to the reduction of China’s
AHGI. In the future, improving the level of AHEE through GHG emissions reduction technology and
narrowing the inter-provincial gap of the level of AHPE are two important paths for promoting the
reduction of China’s AHGI.

Keywords: LMDI; provincial contribution; emission reduction; decomposition; driving factor

1. Introduction
In 2015, at the “Paris Climate Conference”, the international community reached a legally-binding
target of limiting the global temperature increase to no more than 2 ◦ C [1]. To attain this target, global
greenhouse gas (GHG) emissions must be reduced by 70% by 2050 [2]. Moreover, the implementation
of effective emission reduction depends on the emission reduction policies and cooperation of different
countries and their economic sectors [3]. China is the world’s largest emitter of GHG and largest
developing country [4]. The Chinese government had integrated emission reduction with economic
development and promised the world that by 2030 the CO2 emission intensity of its GDP would be

Sustainability 2018, 10, 2492; doi:10.3390/su10072492 47 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 2492

reduced by 60–65% compared to 2005 levels [5]. Meanwhile, this carbon intensity (CI) reduction target
was allocated to each province in order to be achieved [6–8].
However, China’s daunting CI reduction target is only intended for CO2 emissions, with no
clear quantitative target for non-CO2 GHG emission reduction [4]. In fact, non-CO2 GHG emissions
are an important contributor to global warming [9], and the animal husbandry (AH) sector has been
universally recognized as the primary source of global non-CO2 GHG (CH4 and N2 O) emissions [9–13].
Non-CO2 emissions directly from the AH sector contribute approximately 19% to the current climate
warming [14], but there is also very large potential for emission reduction [10,15–18]. China’s AH sector
emitted 445 million tons (2005) of non-CO2 GHG (CO2 equivalents), accounting for approximately 6%
of China’s total GHG emissions and 30% of the total non-CO2 GHG emissions [19]. With the continuous
rise in the per capita income level and the continuous progress in urbanization in China, the demand
for livestock food in the residents’ diet will continue to grow [20–24]. Thus, the AH sector will play
a more important role in reducing GHG emissions in China. China’s CI reduction targets need to be
allocated to each province to achieve. Therefore, it is of great significance to conduct a study from the
perspective of combining emissions reduction with economic development to uncover the vertical
linkage of change in greenhouse gas emission intensity of animal husbandry sector (AHGI) between
China and its provinces, and evaluate the driving factors of change in AHGI, which will provide an
important basis for formulating provincial AHGI reduction targets for China.
Macro studies on global GHG emission intensity of AH sector have been reported. Caro’s study
found that it was vastly different among countries of the intensity of GHG emission per unit of
economic output value in AH sector in 2010, with the highest intensity occurring in developing
countries, and particularly Africa [11]. Bennetzen’s study showed that GHG emissions per unit
livestock product has decreased by approximately 44% since 1970 in global. The decoupling of
livestock production and emissions had shown very large regional differences. While developing
countries have contributed to the doubling of global livestock production, they have also contributed
more GHG emissions [25,26]. However, more literature has focused on the study of the carbon footprint
of animal products from a small scale perspective [27–32].
Existing studies on the vertical linkage and its drivers of CI between China and its provinces have
mainly focused on energy-related CO2 emission intensity [7,33–35], with the logarithmic mean Divisia
index (LMDI) approach being the most commonly used decomposition method. Wang et al. [7] used the
LMDI method to investigate the contribution given by China’s 30 provinces to the decline of national
CI from 1997 to 2008. The results showed that Liaoning, Heilongjiang, and Hebei have made greater
contributions to the decline of national CI, the contribution of a province to the decline of national CI
laid mainly in the promotion of its energy efficiency. Zhang et al. [33] applied the LMDI technique to
explore the CI drivers in 29 Chinese provinces from 1995 to 2012. The results indicated that the overall
CI of China decreased rapidly and energy intensity is the most significant driver for the decrease of CI.
Tan et al. [34] examined the role of activities related to the electric power industry in reducing China’s
CI from 1998 to 2008 utilizing the LMDI technique. The results revealed that the provinces with higher
emission levels contributed the most to China’s improvements in CI. Wang et al. [35] established panel
data models to explore the influencing factors of CI in China. The results showed that the economic
level of activity was negatively correlated to CI on both national and regional levels. However,
attention has not been paid to China’s AH sector. The existing research literature related to China’s AH
sector have either focused more on the macro horizontal perspective on the regional characteristics of
emissions and intensity in various provinces [36–39] and the decomposition of the drivers for carbon
emissions [39–43], or on the micro perspective on the differences in the carbon footprint between
different feeding methods [44,45] and different animal products [46–48]. Meng et al. [36] estimated
the AH’s GHG emissions of China’s different livestock division by life circle assessment method.
The results revealed that there were higher emissions of CO2 equivalent of livestock in agricultural
areas than in pastoral areas, but the emission intensity was lower than in pastoral areas. Yao et al. [37]
used the same method to obtain a conclusion that high livestock carbon emissions areas were mostly

48
Sustainability 2018, 10, 2492

located in prairie areas or major grain producing areas of China. Luo et al. [38] explored the spatial
and temporal heterogeneity of CO2 emission intensity in China’s agricultural sector and found that
Central China had the highest agricultural CO2 emission intensity than Western and Eastern China.
Tian et al. [39,41] studied regional characteristics and driving factor of agricultural carbon emissions in
China with LMDI model. The results showed that the traditional agricultural provinces, especially the
major crop production areas were the main emission source regions. The efficiency factor, labor factor,
and industry structure factor had strong inhibitory effects on China’s agricultural carbon emissions,
while the economy factor had a strong positive effect. Yao et al. [43] conducted a decomposition study
on the factors affecting the changes of AH carbon emissions based on the LMDI method and found
that AH production efficiency improvement was the most important factor to restrain the sustained
growth of the AH carbon emissions. Xiong et al. [40,42] used the same decomposition method to draw
conclusions that the economy factor was the critical factor to promote the increase in agricultural
carbon emissions in Xinjiang province of China, while the main inhibiting factor was the efficiency
factor. These research results have enriched the body of work on GHG emissions reduction in China’s
AH sector from different perspectives. However, the above-mentioned studies have mostly treated both
the AH sector and crop farming sector as part of the agricultural sector and neglected the particularity
of the AH sector. In fact, first of all, the AH sector differs from the crop farming sector in its production
methods, the economic benefits, the generation mechanism of GHG, and the emission reduction
strategies; secondly, studying the GHG emissions and intensity of the AH sector from the horizontal
perspective of provinces cannot reveal the vertical linkage between the partial and overall changes.
More importantly, vertical linkage is an important basis for the Chinese government to formulate
AHGI reduction targets for all provinces.
Our work is different from the above research in the following respects: First, this study
estimated the GHG emissions (CO2 equivalent) per unit of AH economic output value in China and its
31 provinces from 1997 to 2016. Second, we established a vertical linkage of change in AHGI between
china and its 31 provinces from the perspective of combining emissions reduction with economic
development, and separated the factors affecting the change of AHGI into environmental efficiency,
productive efficiency and economic share. We used the LMDI decomposition method to support
our study, because it was proven to be a feasible tool in achieving complete decomposition without
residuals, allowing subgroup estimations to be aggregated in a consistent manner and performing
attribution analyses on the impact of subcategory estimates [49]. Third, we quantified the contributions
of each province and its three driving factors to the change of China’s AHGI during the period of
1997–2016. This study aims to provide a reference for formulating provincial AHGI reduction targets
for the Chinese government in a more scientific and reasonable way.

2. Materials and Methods

2.1. Estimation of AHGI

This study adopted the GHG emissions (CO2 equivalent) per unit of the AH economic output
value as the AHGI indicator. The formula is shown as follows:

AHGI = AHGE/AHGDP (1)

where AHGI, AHGE, and AHGDP denote greenhouse gas emission intensity of animal husbandry
sector (in tCO2 eq/104 yuan), the sum of greenhouse gas emissions from animal husbandry sector
(in tCO2 eq) and economic output value of animal husbandry sector (104 yuan), respectively. The AHGI
of each province is calculated similarly.
According to the “Guidelines for Compiling Low-carbon Development and Provincial Greenhouse
Gas Inventory” issued by the Department of Climate Change of the National Development and Reform
Commission of China (NDRCC) in 2013 [50], the provincial GHG inventory for AH includes two parts:
CH4 and N2 O emissions in animal manure management and CH4 emissions from animal enteric

49
Sustainability 2018, 10, 2492

fermentation in this study. Due to the vast territory of China, the climate and soil conditions in
different geographical regions have different effects on CH4 and N2 O emissions during the storage and
management of animal manure, so the emissions factors of different emission sources also adopt the
recommended values of the sub-regions in China by the guidelines. The formula is shown as follows:
 
AHECH4 ,manure = ∑ APi × EFCH4 ,manure,i × 10−3 (2)
 
AHEN2 O,manure = ∑ APi × EFN2O,manure,i × 10−3 (3)
 
AHECH4 ,enteric = ∑ APi × EFCH4 ,enteric,i × 10−3 (4)
  
AHGE = AHECH4 ,manure + AHECH4 ,enteric × 25 + AHEN2 O,manure × 298 (5)

where AHECH4, manure represent the sum of the CH4 caused by the manure management, in t CH4 /year;
AHEN2 O, manure represent the sum of the N2 O emissions caused by the manure management, in t
N2 O/year; AHECH4, enteric represents the sum of the CH4 emissions caused by enteric fermentation,
in t CH4 /year; APi is the amount of annual feeding of animal i in head; i include cattle, buffalo,
dairy cows, horses, donkeys, mules, camels, goats, sheep, pigs and poultry in China; Non-ruminant
animals, especially poultry, which have small body weights, produce low CH4 emissions. Therefore,
CH4 emissions from non-ruminant animals are not included in animal enteric fermentation emissions;
EFCH4 ,manure ,i is the CH4 emission factor of manure management of animal i in kg CH4 /head/year,
as shown in Table A1; and EFN2 O,manure ,i is the N2 O emission factor of manure management of animal
i in kg N2 O/head/year, as shown in Table A2; EFCH4 ,enteric ,i is the CH4 emission factor of enteric
fermentation of animal i, in kg CH4 /head/year. The guidelines give the methane emission factors for
enteric fermentation of different animals in different feeding modes (large-scale farming, farmer raising,
and grazing) in China. However, it is difficult to obtain the provincial data of livestock activity by
distinguishing different feeding methods, so the CH4 emission factor for animal enteric fermentation in
this study uniformly adopted IPCC recommendations [51] as shown in Table 1, in kg CH4 /head/year.
In order to facilitate the summation of total greenhouse gas emissions and comparative analysis in
each province, we converted CH4 , N2 O to CO2 equivalent. 25 and 298 are the relative molecular
warming forcing of CH4 and N2 O in a 100-year horizon, respectively [52]. AHGE represent the sum
of greenhouse gas emissions from animal husbandry sector, in tCO2 eq. The AHGE of each province
is calculated similarly. The total amount of AHGE in China is equal to the sum of total AHGE in
31 provinces.

Table 1. The CH4 emission factor for animal enteric fermentation (kg CH4 /head/year).

Livestock Emission Factor Livestock Emission Factor Livestock Emission Factor

Buffalo 55 Mule 10 Sheep 5
Dairy cow 61 Camel 46 Goat 5
Cattle 47 Horse 18 Pig 1
Donkey 10

2.2. Decomposition of AHGI

2.2.1. Decomposing Process

As the total AHGE and AHGDP from China are generated by the AH sectors of the 31 provinces
across the country, this study firstly established a vertical linkage of the AHGI calculation between the
national and provincial AH sectors. The calculation is shown as follows:

31 31
AHGE
AHGI =
AHGDP
= ∑ AHGEi / ∑ AHGDPi (6)
i =1 i =1

50
Sustainability 2018, 10, 2492

The existing studies have shown that changes in China’s CI have been impacted not only by
the changes of CI of provinces but also by changes of the GDP share of the provinces in the national
GDP [7,34]. As China’s AH sector is one of the economic production sectors, changes in its intensity
should also comply with the above assertion. Therefore, the factors that drive the changes in AHGI in
the country are divided into two categories: the AHGI of each province and its share of AHGDP in the
national AHGDP. Formula (6) is decomposed as follows:

31
AHGEi AHGDPi
AHGI = ∑ AHGDPi AHGDP
(7)
i =1

However, the changes of AHGI in various provinces are also impacted by different factors.
The differences in resource endowments, development methods, technical levels, and supporting
policies for the development of AH in various provinces in China determine the inter-provincial
differences in the level of AH production [53]. However, this regional difference can be summarized
as the difference in the level of GHG emissions and economic benefits of each province’s AH sector
from the perspective of the AHGI calculation formula. The most perfect scenario for the development
of AH sector is to reduce the amount of GHG emissions while increasing the economic benefits of
livestock. This is also a sustainable path for AH sector to mitigate and adapt to climate change [54,55].
Therefore, this study classifies the driving factors that drive the changes of AHGI in 31 provinces into
two categories: the animal husbandry environmental efficiency (AHEE) factor (GHG emissions per
unit of production factors; the lower the former is, the higher the environmental efficiency) and the
animal husbandry productive efficiency (AHPE) factor (the input of production factors per unit of AH
output value; the lower the former is, the higher the productive efficiency). Formula (7) is, therefore,
further broken down as follows:
31 31
AHGEi AHBSi AHGDPi
AHGI = ∑ AHBSi AHGDPi AHGDP
= ∑ AHEEi AHPEi AHESi (8)
i =1 i =1

where AHBSi denotes the input of production factors in the AH sector (it can be replaced with the
breeding scale of livestock) in the ith province of China. To make it easier for comparing different
types of livestock in different provinces, the equivalent standardized cattle index is introduced to
estimate the total provincial livestock population. The estimation method and parameters are cited
from [56], one cattle is a standard unit, and the reference parameters for converting other livestock to
standard cattle units are shown in Table 2. AHEEi , AHPEi and AHESi are the three drivers of AHGI
in each province, indicating the ith province’s AHEE (GHG emissions per unit of livestock), AHPE
(livestock input per unit of AHGDP), and AHES (the provincial proportion of the AHGDP in the
national AHGDP).

Table 2. The reference parameters for converting other livestock to standard cattle units.

Livestock Parameters Livestock Parameters Livestock Parameters

Buffalo 1.3 Mule 1 Pig 0.3
Dairy cow 2.6 Camel 1.75 Poultry 0.01
Horse 0.8 Goat 0.2
Donkey 0.6 Sheep 0.25

51
Sustainability 2018, 10, 2492

2.2.2. Calculating Method

After decomposing the AHGI into the above three driving factors, as shown in Equation (8),
next we will present the method used to calculate. Referring to Ang [49], the change of AHGI can be
decomposed using an additive LMDI method as follows:

AHGIT
ln = ΔAHGI = AHGIT − AHGI0 = ΔAHEE + ΔAHPE + ΔAHES (9)
AHGI0

where T represents the end of the period; 0, the start of the period; ΔAHGI, the change of AHGI in
China; ΔAHEE, the contribution of AHEE factor; ΔAHPE, the contribution of AHPE factor; and ΔAHES,
the contribution of AHES factor. ΔAHEE, ΔAHPE and ΔAHES can be calculated by:

31
∗
ΔAHEE = ∑ wiAH ln( AHEEi,T /AHEEi,0 ) (10)
i =1

31
∗
ΔAHPE = ∑ wiAH ln( AHPEi,T /AHPEi,0 ) (11)
i =1
31
∗
ΔAHES = ∑ wiAH ln( AHESi,T /AHESi,0 ) (12)
i =1
∗
where wiAH in the above equations is the logarithmic weighting scheme specified in the following:

∗
  31  
wiAH = L wi,0
AH AH
, wi,T / ∑ L wi,0
AH AH
, wi,T (13)
i =1

     
AH
L wi,0 AH
, wi,T = wi,T
AH
− wi,0
AH AH
/ln wi,T AH
/wi,0 (14)

31
wiAH = AHEEi AHPEi AHESi / ∑ AHEEi AHPEi AHESi (15)
i =1

2.3. Data Collection and Processing

This study involves 31 provinces in mainland China and the study period spans from 1997 to
2016. Considering the feeding cycles which are more than one year of cattle, buffalo, dairy cows,
horses, donkeys, mules, goats, and sheep [51], the data for the annual total livestock raised is denoted
by the year-end inventory data. The feeding cycle for poultry (55 days) and pig (200 days) is less
than one year [37], and the data for the annual total is expressed by the current year’s slaughter
volume [53]. The time-series livestock activity data of each province used in this paper are obtained
from the China Rural Statistical Yearbook (1998–2017). The time-series livestock economic output data
of every province are obtained from the China Statistical Yearbook (1998–2017) and then converted to
outputs in constant 1997 price. All abbreviations used in this study are described in Table A3.
As China’s CI reduction target is a long-term target, until 2030, this study took 1997 as the baseline
period and 2016 as the comparison period as the basis for this research.

3. Results and Discussion

3.1. Changes of AHGI in China and Its Provinces

From a national perspective, the AHGI of China decreased from 5.49 tCO2 eq/104 yuan in 1997 to
2.59 tCO2 eq/104 in 2016, showing a 75.25% reduction within this period, as shown in Figure 1. This is in
line with the finding by Caro [11] that the AHGI in global developing countries has been on the decline.

52
Sustainability 2018, 10, 2492

From a provincial perspective, compared 2016 with 1997, the AHGI were all decreasing in
31 provinces, but the extent of the decrease varied significantly among the provinces. Figure 2 shows
that the AHGI in 15 provinces (including Hainan, Heilongjiang, Yunnan, Anhui, Henan, Guizhou,
Shanxi, Hebei, Shaanxi, Guangxi, Xinjiang, Inner Mongolia, Jilin, Shandong and Sichuan) declined
faster than 75.25% (the aggregate reduction in AHGI of China), while the AHGI in other 16 provinces
declined slower than 75.25%. Hainan’s AHGI declined from 6.68 tCO2 eq/104 yuan to 1.76, which was
the largest decline (133.28%) of all the provinces. Liaoning’s AHGI declined from 3.11 tCO2 eq/104 yuan
to 2.54, which was the smallest decline (19.91%) of all the provinces.
According to the above changing trends of the AHGI in China and its provinces during the
period of 1997–2016, this paper argues that these reductions of the AHGI are due to two reasons.
On the one hand, the AHGE has been growing slowly with the transformation of China’s AH
production from an extensive mode to an intensive mode during the study period. On the other hand,
the AHGDP has been growing rapidly due to advancement of livestock feeding and management
techniques, and standardization, scale, and organizational level of AH production. However, there are
significant inter-provincial differences in resource endowments, development methods, technical levels,
and supporting policies for the development of AH, which made the extent of reduction different
among the 31 provinces.

6.0
AHGI (tCO2 eq/104 Yuan)

5.0

4.0

3.0

2.0

1.0

0.0
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016

Year

Figure 1. Changes of AHGI in China during the period 1997–2016.

0.00
-20.00
-40.00
∆AHGI (%)

-60.00
-80.00
-100.00
-120.00
∆AHGI of Province ∆AHGI of China
-140.00
Shandong

Hunan

Tibet
Xinjiang

Chongqing

Liaoning
Beijing
Guangdong

Inner Mongolia
Hebei

Guizhou
Jiangxi

Jiangsu

Qinghai

Gansu

Zhejiang

Shanghai
Sichuan

Shanxi

Hainan

Tianjin
Yunnan

Hubei

Heilongjiang

Jilin
Shaanxi

Fujian

Ningxia
Guangxi

Anhui
Henan

Figure 2. Changes of AHGI in 31 provinces, comparing 2016 with 1997.

It was reported that 445 million tCO2 eq were emitted from animal enteric fermentation and
manure management in the Second National Communication on Climate Change (NCCC) issued by
the Chinese government in 2005, using 21 and 310 as the values for Global Warming Potential (GWP)

53
Sustainability 2018, 10, 2492

of CH4 and N2 O [19]. Our estimates of 503 million tCO2 eq emissions for the corresponding year are
comparable to these data and differences can be attributed to different GWP (this paper used IPCC
Fourth Assessment Report value (25 and 298 of CH4 and N2 O)) [52]. However, this will not affect the
overall research results and, thus, the estimated value of AHGI used in this study is reliable.

3.2. Analysis of Provincial Contributions to the Reduction of China’s AHGI

Compared 2016 with 1997, China’s AHGI showed a 75.25% reduction. The decomposition
results (Table 3, Figure 3) of provincial contributions from the LMDI model showed that all provinces
played a positive role in promoting the 75.25% reduction of China’s AHGI, but there were significant
differences among provinces in the extent of the contribution. The top 10 contributing provinces
were Henan (−7.11%), Hebei (−5.58%), Shandong (−5.55%), Sichuan (−5.29%), Guangxi (−4.81%),
Hunan (−4.29%), Anhui (−4.24%), Yunnan (−3.31%), Guangdong (−3.23%), and Hubei (−2.82%),
while the bottom ten contributing provinces, in descending order, were Tianjin (−0.06%), Ningxia
(−0.14%), Beijing (−0.34%), Liaoning (−0.35%), Shanghai (−0.58%), Hainan (−0.59%), Fujian (−1.01%),
Zhejiang (−1.01%), Chongqing (−1.12%), and Gansu (−1.25%). Considering the largest and smallest
contributors, Henan contributed approximately 119 times as much as Tianjin.

0.00
-1.00
-2.00
Contribution(%)

-3.00
-4.00
-5.00
-6.00
-7.00
-8.00
Shandong

Xinjiang

Liaoning
Hunan

Tibet

Chongqing

Beijing
Hebei

Guangdong

Guizhou

Inner Mongolia

Qinghai
Jiangsu
Sichuan

Jiangxi

Heilongjiang

Shanxi

Gansu

Zhejiang

Shanghai
Hainan

Tianjin
Yunnan

Hubei

Jilin
Shaanxi
Guangxi

Anhui

Fujian

Ningxia
Henan

Figure 3. Provincial contributions to the reduction of China’s AHGI, comparing 2016 with 1997.

The study period witnessed a decline of the AHGI in all provinces, which contributed positively
to the reduction in national AHGI. However, the results of linear regression between the reduction of
AHGI in 31 provinces and the contributions of 31 provinces to the country showed that the R2 value was
only 0.1543 (Figure 4). This showed that there was an inconsistency between the extent of the actual
reduction of AHGI in each province and its contributions to the country. Taking Hainan and Hunan as
an example, the actual decline in AHGI in Hainan (133.28%) is the highest in 31 provinces, but Hainan’s
contribution (0.59%) to the reduction of China’s AHGI is ranked the reciprocal sixth position among all
provinces. The decline in AHGI in Hunan (56.74%) is only ranked 24th, but its contribution (4.29%)
is ranked sixth among all provinces. The reason is that the proportion of AH scale, GHG emissions,
and share of the output value in Hainan are relatively small relative to the entire country (0.75%, 0.75%,
and 1.11% in 2016, respectively). This is reflected in the LMDI decomposition model of this study as
a smaller weighting factor. Consequently, the actual decline in AHGI in Hainan has less impact on the
decline in national AHGI. Likewise, the proportion of the above-mentioned three factors in Hunan are
relatively large in the country (5.21%, 5.68%, and 6.27% in 2016), which makes Hunan have a greater
impact on the decline in national AHGI. Similar provinces include Sichuan, Guangdong, Shaanxi,
and Shanxi. This indicates that the proportion of the provincial AH scale, GHG emissions, and share of
economic output value in the country are important for measuring their contributions.

54
Sustainability 2018, 10, 2492

ǻAHGI 
-140.00 -120.00 -100.00 -80.00 -60.00 -40.00 -20.00 0.00
0.00
-1.00

-2.00

Contribution (%)
-3.00

-4.00

-5.00

-6.00
y = 0.0252x - 0.5545
R² = 0.1543 -7.00

-8.00

Figure 4. The scatter diagram of the regression variables between the change of AHGI in 31 provinces
and the contributions of the 31 provinces to the country.

In terms of the regional characteristics of animal husbandry production, among the top
10 contributing provinces, Henan, Hebei, Shandong, Sichuan, Hunan, Anhui, and Hubei are the major
grain-producing regions in China, and they are also the major livestock breeding provinces in the
agricultural areas of China. There are abundant feeding resources from crops, and the standardization,
scale, and organizational level of AH production are high in these provinces. They are currently China’s
main base for producing livestock such as live pigs, beef cattle, and poultry [53,57], and shoulder the
important function of supplying animal-based food to the country; the top ten provinces cumulatively
contributed to a reduction of 46.22% in China’s AHGI, accounting for 61.42% of the total contributions
by 31 provinces. Meanwhile, for these provinces in 2016, it accounted for approximately 55.16%, 55.01%,
and 61.05% of the scale of livestock breeding, AHGE, and AHGDP, respectively, of the corresponding
total amount in the country.
Among the bottom ten contributing provinces, Beijing, Tianjin, Shanghai, and Chongqing are the
four municipalities directly governed by the Chinese government. Zhejiang, Fujian, Hainan, and Liaoning
are the coastal provinces of Eastern China. The above eight provinces and municipalities are the major
consumers of animal-based food in China. They are densely populated, with relatively high levels of
urbanization and industrialization, and their AH production is dominated by modern urban AH [37]
and the proportion of AHGDP in the GDP is relatively low; in contrast, Gansu and Ningxia are in the
northwest agro-pastoral ecotone of China, with a relatively fragile ecological environment, and strong
resource and environment constraints for the development of AH, and the total output from AH is not
large [24,58]. The bottom ten provinces cumulatively contributed to a reduction of only 6.45% in China’s
AHGI, accounting for 8.57% of total provincial contributions. Meanwhile, for these provinces in 2016,
it accounted for approximately 14.39%, 12.97% and 13.07% of the scale of livestock breeding, AHGE,
and AHGDP, respectively, of the corresponding total amount in the country.
The remaining 11 provinces cumulatively contributed to a reduction of 22.58% in China’s AHGI,
accounting for 30.01% of the provincial total contributions. Among these provinces, Inner Mongolia,
Xinjiang, Qinghai, and Tibet are the traditional pastoral areas, with a long development history of
AH. With rich resources in natural grassland, the focus is primarily on the development of grassland
AH. They are currently China’s major breeding base for cattle, sheep, horses, and other herbivorous
livestock [58]; on the other hand, Jiangxi, Heilongjiang, Jiangsu, and Jilin are the main grain-producing
regions in China and are rich in feed resources, the focus is primarily on the development of AH
in agricultural areas. For these provinces in 2016, it accounted for approximately 30.45%, 32.02%,
and 25.88% of the scale of livestock breeding, AHGE, and AHGDP, respectively, of the corresponding
total amount in the country.

55
Sustainability 2018, 10, 2492

The discussion above showed that there was an inconsistency between the extent of the actual
reduction of AHGI in each province and their contributions to the country, China’s progress in reducing
AHGI was mainly made by provinces with a large GHG emissions from AH. The conclusion drawn by
this study that provinces contributed to the reduction in national CI is consistent with the conclusion
drawn by Tan’s research [34] on the Chinese power industry and Wang’s research [7] on China’s
economic development. The revelation for us is that the government should comprehensively consider
the actual decline of AHGI in all provinces and its contributions to the reduction in national AHGI
in formulating provincial AHGI reduction targets for China. Each province should not be required
to have the same decline in AHGI as in the national AHGI. In addition, priority should be given to
assessing the emission reduction responsibilities and impact in large AH provinces, because while
these provinces emit a larger share of AHGE, they also supply a larger share of animal-based food
and create a larger share of AHGDP for the country. More importantly, these provinces are also major
contributors in reducing the AHGI of China.

3.3. Analysis of Driving Factors’ Contributions to the Reduction of China’s AHGI

The decomposition results of three driving factors’ contributions from the LMDI model (Table 3,
Figure 5) indicate that there is a complex linkage among the three driving factors: AHEE, AHPE,
and AHES. Three driving factors comprehensively determine the reduction of China’s AHGI through
two different contributions of positive promotion and negative inhibition, but the way the three driving
factors exert impact and the extent of their contributions vary significantly among provinces. Overall,
the AHPE factors of all provinces are the main factors contributing to the reduction of China’s AHGI,
cumulatively contributing to 68.17%, followed by the AHEE factors (11.78%). The AHES factors of
various provinces have the nature of a “double-edged sword”, having cumulatively inhibited the
4.70% reduction of China’s AHGI.

Table 3. The decomposition results of vertical linkage of changes in AHGI between China and its
provinces based on the LMDI model.

The Decomposition Results of Three The Decomposition Results of Three

Province Driving Factors (%) Province Driving Factors (%)
ΔAHEE ΔAHPE ΔAHES Total ΔAHEE ΔAHPE ΔAHES Total
China −11.78 −68.17 4.70 −75.25 Jiangsu −0.15 −1.05 −0.94 −2.15
Henan −2.17 −6.93 1.99 −7.11 Heilongjiang −0.34 −3.29 1.63 −2.00
Hebei −0.52 −4.96 −0.09 −5.58 Qinghai 0.07 −1.82 −0.15 −1.90
Shandong −1.25 −4.62 0.32 −5.55 Shanxi −0.29 −1.25 −0.01 −1.55
Sichuan −0.47 −5.67 0.85 −5.29 Jilin −0.15 −1.97 0.57 −1.55
Guangxi −1.17 −3.40 −0.23 −4.81 Shaanxi −0.23 −1.13 0.06 −1.31
Hunan −0.27 −2.96 −1.05 −4.29 Gansu 0.02 −1.36 0.10 −1.25
Anhui −1.43 −2.54 −0.27 −4.24 Chongqing −0.16 −0.58 −0.38 −1.12
Yunnan −0.53 −4.74 1.96 −3.31 Zhejiang −0.08 −0.26 −0.66 −1.01
Guangdong −0.26 −2.08 −0.88 −3.23 Fujian −0.44 −0.03 −0.54 −1.01
Hubei −0.52 −2.11 −0.19 −2.83 Hainan −0.30 −0.72 0.43 −0.59
Guizhou −0.44 −2.90 0.63 −2.71 Shanghai 0.07 −0.24 −0.41 −0.58
Jiangxi −0.66 −1.29 −0.56 −2.51 Liaoning −0.07 −0.47 0.19 −0.35
Tibet 0.10 −1.90 −0.53 −2.33 Beijing 0.04 −0.11 −0.27 −0.34
Xinjiang −0.22 −3.00 0.91 −2.31 Ningxia 0.06 −0.44 0.25 −0.14
Inner Mongolia 0.02 −4.14 1.86 −2.26 Tianjin −0.02 −0.20 0.16 −0.06
Note: Positive and negative values in the table represent the contribution of two different properties, the positive
value is the contribution to inhibit the reduction of China’s AHGI, while negative value is the contribution to
promote the reduction of China’s AHGI.

56
Sustainability 2018, 10, 2492

2.50

0.50
Contribution (%)

-1.50

-3.50

-5.50

-7.50
∆AHEE ∆AHPE ∆AHES
-9.50
Shandong

Xinjiang
Hunan

Tibet

Chongqing

Beijing
Guangdong

Liaoning
Guizhou

Inner Mongolia

Qinghai
Hebei

Jiangsu
Sichuan

Jiangxi

Tianjin
Shanxi

Gansu

Zhejiang

Shanghai
Hainan
Yunnan

Hubei

Heilongjiang

Jilin
Shaanxi

Ningxia
Guangxi

Anhui

Fujian
Henan

Figure 5. Driving factors’ contributions to the reduction of AHGI in each province, comparing 2016 with 1997.

3.3.1. AHPE Factor

With the transformation of China’s AH production from an extensive mode to an intensive
mode and the continuous improvement in the productivity of AH, the livestock input for China’s
10,000 yuan of AHGDP dropped from the 5.98 standard cattle in 1997 to 3.17 standard cattle in 2016,
and the level of AHPE increased about 63.47%. The livestock input for 10,000 yuan of AHGDP
in all provinces of China also decreased (Figure 6). As a result, the AHPE factors of all provinces
contributed positively to the reduction of AHGI. Among them, Henan’s contribution (6.93%) was the
highest, and Tianjin’s contribution (0.20%) was the lowest. Overall, the AHPE factors of all provinces
cumulatively contributed to a reduction of 68.17% in AHGI of China. However, due to the vast territory
of China, there are significant regional differences among provinces in terms of the economic benefits
of livestock products. Taking 2016 as an example, the livestock input for 10,000 yuan of AHGDP for
China’s frontier grassland pastoral areas (Tibet (28.59), Qinghai (15.20), Gansu (7.72), Xinjiang (7.20),
Inner Mongolia (4.75), Ningxia (4.63), Guizhou (4.18), Yunnan (4.14), and Guangxi (3.73)) was higher
than the national average (3.17) due to the comprehensive impact of the productivity level of AH,
the distance to the consumer market of livestock products, and the national dietary habits [24]. On the
other hand, the livestock input for 10,000 yuan of AHGDP for China’s central and eastern regions
(Henan (2.55), Anhui (2.47), Hubei (2.62), (Jiangsu (2.40), Zhejiang (2.35), and Tianjin (1.46)), which are
close to the consumer market, have a larger scale of AH, and a higher intensity, was lower than the
national average. This finding shows that the AHPE factor of each province is the leading factor in
promoting the reduction of China’s AHGI, but there are still large gaps among provinces. Overall,
the productive efficiency level of China’s frontier grassland pastoral areas is lower than that of central
and eastern provinces.

3.3.2. AHEE Factor

The GHG emissions per unit standard cattle in China dropped from 0.92 tCO2 eq in 1997 to
0.82 tCO2 eq in 2016, and the level of AHEE increased about 11.51%. However, the changes of
AHEE levels were different in 31 provinces (Figure 6), as a result, the AHEE factors of each province
have both positive and negative contributions in reducing the China’s AHGI. Among 31 provinces,
the GHG emissions per unit standard cattle in these seven provinces (Tibet (1.16 increased to 1.20),
Qinghai (1.05 increased to 1.08), Inner Mongolia (0.895 increased to 0.899), Ningxia (0.81 increased to
0.89), Gansu (0.89 increased to 0.90), Beijing (0.62 increased to 0.70), and Shanghai (0.59 increased to
0.75)) increased slightly, which cumulatively inhibited the 0.38% reduction of China’s AHGI. On the
one hand, Shanghai and Beijing are currently China’s cities with relatively developed economy and
urbanization among the seven provinces. As the demand of urban residents for milk consumption

57
Sustainability 2018, 10, 2492

continues to grow, the proportion of dairy cows in their livestock breeding structure has been increasing,
resulting in an increase in emissions. On the other hand, Tibet, Qinghai, Inner Mongolia, Ningxia,
and Gansu are China’s traditional grassland pastoral regions, so their livestock breeding focuses
mainly on cattle, sheep, horses, and other ruminant livestock. The methane emissions generated by
the enteric fermentation of these animals are relatively high [12,59]. As these livestock breeding scales
increase, so will the amount of emissions. The GHG emissions per unit standard cattle in the remaining
24 provinces have been on the decline, which cumulatively promoted the 12.16% reduction of China’s
AHGI. Overall, the AHEE factors of all provinces only cumulatively promoted the 11.78% reduction of
China’s AHGI. This indicates that the reduction of China’s AHGI during the study period depended
more on the substantial increase in the AHPE of all the provinces than on the improvement of AHEE.

3.3.3. AHES Factor

The AHGDP of China continued to grow from 713.33 billion yuan in 1997 to 1707.90 billion yuan
in 2016, which is a relative increase of 87.31%. The 15 provinces of Henan, Yunnan, Inner Mongolia,
Heilongjiang, Xinjiang, Sichuan, Guizhou, Jilin, Hainan, Shandong, Ningxia, Liaoning, Tianjin, Gansu,
and Shaanxi all saw an increase in their AHES (Figure 6). However, the increase in AHES of these
provinces was significantly faster than the increase in AHEE, which inevitably led to a rapid increase
in carbon emissions when they expanded the scale of AH production. Therefore, the AHES factors
of these provinces all inhibited the reduction of China’s AHGI. However, the AHES in the remaining
16 provinces was on the decline. As the AHES declined, so did the GHG emissions. Therefore,
the AHES factors of these provinces all promoted the reduction of China’s AHGI. However, due to the
difference in the base of AHGDP in each province, the increase and decrease based on the AHGDP
were also different. As a result, the contribution from the AHES factors of different provinces varied.
Overall, the cumulative negative contribution from the AHES factors of 15 provinces, including Henan,
was 11.88%, while the AHES factors of the other 16 provinces, including Anhui, cumulatively made
a positive contribution of 7.18%. In all, the AHES factors of all provinces cumulatively inhibited
a 4.70% reduction of China’s AHGI. This means that, in terms of contributions by each province to the
reduction in China’s AHGI, the AHES factor is a weight with the nature of a “double-edged sword”,
and can decrease or increase the contribution value of each province. If a province can expand its scale
of AH production and also improve the level of AHEE, there will be a greater increase in the AHGDP
of the province, and a greater positive contribution to the reduction in national AHGI. If not, then the
result will be the opposite.

60.00

30.00
Actual change (%)

0.00

-30.00

-60.00

-90.00

-120.00
AHEE AHPE AHES
-150.00
Shandong

Beijing
Hunan

Tibet
Xinjiang

Chongqing
Guangdong

Liaoning
Guizhou

Inner Mongolia

Qinghai
Hebei

Jiangsu

Shanghai
Sichuan

Jiangxi

Heilongjiang

Shanxi

Gansu

Zhejiang

Hainan

Tianjin
Yunnan

Hubei

Jilin
Shaanxi
Guangxi

Anhui

Fujian

Ningxia
Henan

Figure 6. Actual change of three driving factors in each province of China, comparing 2016 with 1997.

58
Sustainability 2018, 10, 2492

Currently, China is the foremost producer of GHG emissions and largest developing country in the
world. China is also a major producer of livestock products in the world. China’s AH sector not only
shoulders responsibility for supplying livestock products to more than 1.3 billion people, but also takes
care of the livelihoods of more than 200 million farmers and herdsmen. With the continuous rise in the
per capita income level and the continuous progress of urbanization in China, the demand for livestock
food in the residents’ diet will continue to increase. Therefore, it is an objective need and an inevitable
trend for various provinces in China to expand the scale of breeding and pursue economic benefits of AH.
In terms of the driving factors that contribute to the reduction of China’s AHGI during the research period,
AHPE factors played a major role. However, in terms of the reduction responsibilities of the AH sector
in China, the development of AH should take into account both economic and environmental benefits.
The most perfect scenario for the development of AH sector is to reduce the amount of GHG emissions
while increasing the economic benefits of livestock [54,55]. This is also a sustainable path for China’s AH
sector to mitigate and adapt to climate change. With reference to Caro’s results [11], the AHGI of China in
2010 (2.87 tCO2 eq/104 yuan) was much lower than that of Vietnam (17.97 tCO2 eq/104 yuan) and India
(16.16 tCO2 eq/104 yuan), both of which have higher emission intensities in Asia, but it is 3.78 times that of
the United States (0.76 tCO2 eq/104 yuan). This shows that although the AHGI has been continuously on
the decline, there is still a large gap compared with the developed countries, and there is still more room
for greater emissions reduction in the future. On the one hand, Wang’s research shows that the greatest
technical emission reduction potential for China’s AH sector will be 253 Mt of CO2 emission by 2020 [60],
accounting for 56.85% of total GHG emissions in 2005 from AH. This shows that the technical means will
be important measures to reduce GHG emissions for China’s AH sector in the future. On the other hand,
Herrero’s research indicates that GHG emissions can be effectively reduced in AH sector by using feed
additives to improve the animal’s forage digestibility and strengthening the storage and management
of animal manure and other technical means [15]. Therefore, in the future, all provinces should focus
more on improving the level of AHEE, and further reduce the GHG emissions of livestock by improving
the raising of livestock and manure management technologies so as to promote the conversion from
advantage in production scale to advantage in contribution to emissions reduction. In addition, there is
a large gap among all provinces in China in terms of AHPE. Therefore, narrowing the inter-provincial gap
of AHPE is also an important path for promoting the reduction of China’s AHGI.

3.4. Advantages and Limitations of This Study

This study focused on AHGI reduction in China and its provinces. Compared with previous
studies, this study went deeper in the following three aspects. First, on the decomposition scale, it
was different from the existing decomposition studies on the GHG emissions from AH [39,41–43],
which have been done only from the horizontal provincial scales. This study firstly established
a vertical linkage of change in AHGI between china and its 31 provinces and clearly revealed the
linkage between partial changes and overall changes. This is more in line with China’s current need
to allocate GHG reduction tasks from top to bottom. Second, in terms of driving factors, the existing
studies have mostly explained the impact on GHG emissions of AH [39,41–43]. Based on the AHGI
calculation formula, we separated the factors affecting the change of China’s AHGI into environmental
efficiency, productive efficiency, and economic share. Our research effectively combined emissions
reduction and economic development, thus, it can provide a more specific basis for each province to
formulate GHG emission reduction measures for the AH sector. Third, in terms of research findings,
previous studies [36–39] found that provinces such as Henan, Shandong, Hebei, and Sichuan have
always been major contributors to GHG emissions from the AH sector in China. Our findings indicated
that these provinces were not only major contributors to GHG emissions from the AH sector in China,
they were also the main contributors to the reduction of China’s AHGI. This is of great significance for
a comprehensive and objective understanding of the responsibilities of the provinces with large GHG
emissions for their emissions reduction tasks.

59
Sustainability 2018, 10, 2492

However, although there are some advantages in the study, it also needs for further development.
First, we only discussed the decomposition results of provincial contributions to the reduction of
China’s AHGI comparing 2016 with 1997. However, we did not further divide the study period into
different time periods for detailed analysis and discussion. Future studies should strengthen the
comparative analysis at different time periods. In addition, we only revealed the linkage of AHGI
change between china and its 31 provinces, but did not delve more deeply into the issues of fairness
and efficiency of contribution values in each province. In future research, the LMDI decomposition
method and the performance evaluation method should be combined to answer the issues of fairness
and efficiency of each province’s contribution value. Three major factors, which are the reduction of
greenhouse gas emissions, economic growth and the supply of livestock food, should be included in
the performance evaluation system together.

4. Conclusions
This study established a vertical linkage of GHG emission intensity change of the animal
husbandry sector between China and its 31 provinces based on LMDI decomposing method from the
perspective of combining emission reductions with economic development. In addition, the study
quantified the contributions of each province and its three driving factors of environmental efficiency,
productive efficiency, and economic share to reducing China’s animal husbandry GHG emission
intensity during the period of 1997–2016. The final conclusions are as follows.

(1) The AHGI of China decreased from 5.49 tCO2 eq/104 yuan in 1997 to 2.59 tCO2 eq/104 in 2016,
showing a 75.25% reduction. Compared 2016 with 1997, the AHGI in 31 provinces also declined and
played a positive role in promoting the reduction of the national AHGI, but there were significant
differences among provinces in the extent of contribution. Henan, the largest contributor, contributed
to a 7.11% reduction of China’s AHGI, and Tianjin was the smallest contributor (0.06%). The top ten
provinces (Henan, Hebei, Shandong, Sichuan, Guangxi, Hunan, Anhui, Yunnan, Guangdong and
Hubei) cumulatively contributed to a reduction of 46.22% in China’s AHGI, accounting for 61.42%
of the total contributions by 31 provinces; while the bottom ten provinces (Tianjin, Ningxia, Beijing,
Liaoning, Shanghai, Hainan, Fujian, Zhejiang, Chongqing and Gansu) cumulatively contributed to
a reduction of only 6.45% in China’s AHGI, accounting for 8.57% of total provincial contributions.
Overall, there was an inconsistency between the extent of the actual reduction of AHGI in each
province and its contributions to the country. China’s progress in reducing AHGI was mainly made
by provinces with a large GHG emissions from AH.
(2) Three driving factors (environmental efficiency, productive efficiency, and economic share)
comprehensively determine the reduction of China’s AHGI through two different contributions of
positive promotion and negative inhibition, but the way in which the three driving factors exert their
impact and the extent of their contributions vary significantly among provinces. The productive
efficiency and environmental efficiency factors in 31 provinces cumulatively contributed to the
respective 68.17% and 11.78% reduction of China’s AHGI, while the economic share factors of
31 provinces cumulatively inhibited the 4.70% reduction of China’s AHGI. Overall, the productive
efficiency factors are the main driving factors contributing to the reduction of China’s AHGI.
The reduction of China’s AHGI during the study period depended more on the substantial increase
in the AH’s productive efficiency than on the improvement of AH’s environmental efficiency.
The economic share factor was a weight with the nature of a “double-edged sword”, which can
decrease or increase the contribution value of each province to the reduction of China’s AHGI. In the
future, improving the level of AHEE through GHG emission reduction technology and narrowing
the inter-provincial gap of the level of AHPE are two important paths for promoting the reduction of
China’s AHGI. In terms of improving the level of AHEE, all provinces need to do this. However this is
even more urgent in the seven provinces, including Tibet, Qinghai, Inner Mongolia, Ningxia, Gansu,
Beijing and Shanghai. In terms of narrowing the inter-provincial gap of the level of AHPE, the gap is
mainly reflected between the frontier grassland pastoral areas in the western and the agricultural

60
Sustainability 2018, 10, 2492

areas in Central and Eastern China. The key provinces that need to improve the level of AHPE
are located in grassland pastoral areas, including Tibet, Qinghai, Gansu, Xinjiang, Inner Mongolia,
Ningxia, Guizhou, Yunnan and Guangxi.

Author Contributions: T.C. and D.Y. designed the research; T.C., D.Y., and F.X. performed the research;
R.W. analyzed the data; T.C. drafted the manuscript, which was revised by D.Y. and X.Z. All authors have
read and approved the final manuscript.
Funding: This research was funded by Grant Program of Clean Development Mechanism Fund of China (CDMF)
grant number [No. 2014092].
Acknowledgments: We acknowledge the Grant Program of Clean Development Mechanism Fund of China
(CDMF) (No. 2014092).
Conflicts of Interest: The authors declare no conflict of interest.

Appendix A

Table A1. The CH4 emission factor for animal manure management (kg CH4 /head/year).

Region Dairy Cow Cattle Buffalo Horse Donkey Mule

North China 7.46 2.82 - 1.09 0.60 0.60
Northeast China 2.23 1.02 - 1.09 0.60 0.60
East China 8.33 3.31 5.55 1.64 0.90 0.90
Central and Southern China 8.45 4.72 8.24 1.64 0.90 0.90
Southwest China 6.51 3.21 1.53 1.64 0.90 0.90
Northwest China 5.93 1.86 - 1.09 0.60 0.60
Region Camel Sheep Goat Pig Poultry
North China 1.28 0.15 0.17 3.12 0.01
Northeast China 1.28 0.15 0.16 1.12 0.01
East China 1.92 0.26 0.28 5.08 0.02
Central and Southern China 1.92 0.34 0.31 5.85 0.02
Southwest China 1.92 0.48 0.53 4.18 0.02
Northwest China 1.28 0.28 0.32 1.38 0.01
Note: North China: Beijing, Tianjin, Hebei, Shanxi, Inner Mongolia; Northeast China: Heilongjiang, Jilin, Liaoning;
East China: Shanghai, Jiangsu, Zhejiang, Anhui, Fujian, Jiangxi, Shandong; Central and Southern China: Henan,
Hubei, Hunan, Guangxi, Guangdong, Hainan; Southwest China: Chongqing, Sichuan, Guizhou, Yunnan, Tibet;
Northwest China: Shaanxi, Gansu, Ningxia, Qinghai, Xinjiang.

Table A2. The N2 O emission factor for animal manure management (kg N2 O/head/year).

Region Dairy Cow Cattle Buffalo Horse Donkey Mule

North China 1.846 0.794 - 0.330 0.188 0.188
Northeast China 1.096 0.931 - 0.330 0.188 0.188
East China 2.065 0.846 0.875 0.330 0.188 0.188
Central and Southern China 1.710 0.805 0.860 0.330 0.188 0.188
Southwest China 1.884 0.691 1.197 0.330 0.188 0.188
Northwest China 1.447 0.545 - 0.330 0.188 0.188
Region Camel Sheep Goat Pig Poultry
North China 0.330 0.093 0.093 0.227 0.007
Northeast China 0.330 0.057 0.057 0.266 0.007
East China 0.330 0.113 0.113 0.175 0.007
Central and Southern China 0.330 0.106 0.106 0.157 0.007
Southwest China 0.330 0.064 0.064 0.159 0.007
Northwest China 0.330 0.074 0.074 0.195 0.007
Note: The provinces included in different regions are the same as Table A1.

61
Sustainability 2018, 10, 2492

Table A3. Abbreviations.

Item Descriptions
GHG Greenhouse gas
AH Animal husbandry
CI Carbon intensity
LMDI The logarithmic mean Divisia index
AHGI Greenhouse gas emission intensity of animal husbandry sector (in tCO2 eq/104 yuan)
AHGE The sum of greenhouse gas emissions from animal husbandry sector (in tCO2 eq)
AHGDP Economic output value of animal husbandry sector (104 yuan)
The input of production factors in the animal husbandry sector (it can be replaced with the breeding scale
AHBS
of livestock by converting to standard cattle units)
AHEE The animal husbandry environmental efficiency (GHG emissions per unit of livestock)
AHPE The animal husbandry productive efficiency (livestock input per unit of AHGDP)
AHES The animal husbandry economic share (the provincial proportion of the AHGDP in the national AHGDP)

References
1. Vandyck, T.; Keramidas, K.; Saveyn, B.; Kitous, A.; Vrontisi, Z. A global stocktake of the Paris pledges:
Implications for energy systems and economy. Glob. Environ. Chang. 2016, 41, 46–63. [CrossRef]
2. Food and Agriculture Organization (FAO). The State of Food and Agriculture Climate Change, Agriculture and
Food Security; FAO: Rome, Italy, 2016.
3. Intergovernmental Panel on Climate Change (IPCC). Clim. Chang. 2014: Synthesis Report. Contribution of
Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change;
Core Writing Team, Pachauri, R.K., Meyer, L.A., Eds.; IPCC: Geneva, Switzerland, 2014; 151p.
4. Liu, L.-C.; Wu, G. The effects of carbon dioxide, methane and nitrous oxide emission taxes: An empirical
study in China. J. Clean. Prod. 2017, 142, 1044–1054. [CrossRef]
5. National Development and Reform Commission of China (NDRCC). Enhanced Actions on Climate Change:
China's Intended Nationally Determined Contributions; NDRCC: Beijing, China, 2015.
6. Chen, Y.; Lin, S. Decomposition and allocation of energy-related carbon dioxide emission allowance over
provinces of China. Nat. Hazards 2014, 76, 1893–1909. [CrossRef]
7. Wang, F.; Feng, G.; Wu, L. Regional Coutribution to the Decline of National Carbon Intensity in China’s
Economic Growth. Econ. Res. 2013, 8, 143–155.
8. Wang, K.; Zhang, X.; Wei, Y.-M.; Yu, S. Regional allocation of CO2 emissions allowance over provinces in
China by 2020. Energy Policy 2013, 54, 214–229. [CrossRef]
9. Smith, P.M.B.; Ahammad, H.; Clark, H.; Dong, H.; Elsiddig, E.A.; Haberl, H.; Harper, R.; House, J.; Jafari, M.;
Masera, O.; et al. Agriculture, Forestry and Other Land Use (AFOLU). In Climate Change 2014: Mitigation of
Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on
Climate Change; Edenhofer, O., Pichs-Madruga, R., Sokona, Y., Farahani, E., Kadner, S., Seyboth, K., Adler, A.,
Baum, I., Brunner, S., Eickemeier, P., et al., Eds.; Cambridge University Press: Cambridge, UK; New York,
NY, USA, 2014; pp. 811–922.
10. Smith, P.; Martino, D.; Cai, Z.; Gwary, D.; Janzen, H.; Kumar, P.; McCarl, B.; Ogle, S.; O’Mara, F.; Rice, C.;
et al. Greenhouse gas mitigation in agriculture. Philos. Trans. R. Soc. Lond. Ser. B Boil. Sci. 2008, 363, 789–813.
[CrossRef] [PubMed]
11. Caro, D.; Davis, S.J.; Bastianoni, S.; Caldeira, K. Global and regional trends in greenhouse gas emissions from
livestock. Clim. Chang. 2014, 126, 203–216. [CrossRef]
12. Ripple, W.J.; Smith, P.; Haberl, H.; Montzka, S.A.; McAlpine, C.; Boucher, D.H. Ruminants, climate change
and climate policy. Nat. Clim. Chang. 2013, 4, 2–5. [CrossRef]
13. O’Mara, F.P. The significance of livestock as a contributor to global greenhouse gas emissions today and in
the near future. Anim. Feed. Sci. Technol. 2011, 166–167, 7–15. [CrossRef]
14. Reisinger, A.; Clark, H. How much do direct livestock emissions actually contribute to global warming?
Glob. Chang. Boil. 2017, 24, 1749–1761. [CrossRef] [PubMed]
15. Herrero, M.; Henderson, B.; Havlík, P.; Thornton, P.K.; Conant, R.T.; Smith, P.; Wirsenius, S.; Hristov, A.N.;
Gerber, P.; Gill, M.; et al. Greenhouse gas mitigation potentials in the livestock sector. Nat. Clim. Chang. 2016,
6, 452–461. [CrossRef]

62
Sustainability 2018, 10, 2492

16. Havlik, P.; Valin, H.; Herrero, M.; Obersteiner, M.; Schmid, E.; Rufino, M.C.; Mosnier, A.; Thornton, P.K.;
Bottcher, H.; Conant, R.T.; et al. Climate change mitigation through livestock system transitions.
Proc. Natl. Acad. Sci. USA 2014, 111, 3709–3714. [CrossRef] [PubMed]
17. Gerber, P.J.S.H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling Climate
Change through Livestock—A Global Assessment of Emissions and Mitigation Opportunities; Food and Agriculture
Organization of the United Nations (FAO): Rome, Italy, 2013.
18. Frank, S.; Beach, R.; Havlík, P.; Valin, H.; Herrero, M.; Mosnier, A.; Hasegawa, T.; Creason, J.; Ragnauth, S.;
Obersteiner, M. Structural change as a key component for agricultural non-CO2 mitigation efforts.
Nat. Commun. 2018, 9, 1–8. [CrossRef] [PubMed]
19. National Coordination Committee on Climate Change (NCCC). Second National Communication on Climate
Change of The People’s Republic of China; NCCC: Beijing, China, 2012.
20. Tilman, D.; Clark, M. Global diets link environmental sustainability and human health. Nature 2014, 515,
518–522. [CrossRef] [PubMed]
21. Lin, J.; Hu, Y.; Cui, S.; Kang, J.; Xu, L. Carbon footprints of food production in China (1979–2009). J. Clean. Prod.
2015, 90, 97–103.
22. Hawkins, J.; Ma, C.; Schilizzi, S.; Zhang, F. China’s changing diet and its impacts on greenhouse gas
emissions: An index decomposition analysis. Aust. J. Agric. Resour. Econ. 2018, 62, 45–64. [CrossRef]
23. Popp, A.; Calvin, K.; Fujimori, S.; Havlik, P.; Humpenöder, F.; Stehfest, E.; Bodirsky, B.L.; Dietrich, J.P.; Doelmann, J.C.;
Gusti, M.; et al. Land-use futures in the shared socio-economic pathways. Glob. Environ. Chang. 2017, 42, 331–345.
[CrossRef]
24. Li, X.L.; Yuan, Q.H.; Wan, L.Q.; He, F. Perspectives on livestock production systems in China. Rangel. J. 2008,
30, 211. [CrossRef]
25. Bennetzen, E.H.; Smith, P.; Porter, J.R. Decoupling of greenhouse gas emissions from global agricultural
production: 1970–2050. Glob. Chang. Biol. 2016, 22, 763–781. [CrossRef] [PubMed]
26. Bennetzen, E.H.; Smith, P.; Porter, J.R. Agricultural production and greenhouse gas emissions from world
regions—The major trends over 40 years. Glob. Environ. Chang. 2016, 37, 43–55. [CrossRef]
27. Tichenor, N.E.; Peters, C.J.; Norris, G.A.; Thoma, G.; Griffin, T.S. Life cycle environmental consequences of
grass-fed and dairy beef production systems in the Northeastern United States. J. Clean. Prod. 2017, 142,
1619–1628. [CrossRef]
28. Lesschen, J.P.; van den Berg, M.; Westhoek, H.J.; Witzke, H.P.; Oenema, O. Greenhouse gas emission profiles
of European livestock sectors. Anim. Feed. Sci. Technol. 2011, 166–167, 16–28. [CrossRef]
29. Reckmann, K.; Traulsen, I.; Krieter, J. Life Cycle Assessment of pork production: A data inventory for the
case of Germany. Livest. Sci. 2013, 157, 586–596. [CrossRef]
30. Gollnow, S.; Lundie, S.; Moore, A.D.; McLaren, J.; van Buuren, N.; Stahle, P.; Christie, K.; Thylmann, D.;
Rehl, T. Carbon footprint of milk production from dairy cows in Australia. Int. Dairy J. 2014, 37, 31–38.
[CrossRef]
31. Patra, A.K. Accounting methane and nitrous oxide emissions, and carbon footprints of livestock food
products in different states of India. J. Clean. Prod. 2017, 162, 678–686. [CrossRef]
32. Desjardins, R.; Worth, D.; Vergé, X.; Maxime, D.; Dyer, J.; Cerkowniak, D. Carbon Footprint of Beef Cattle.
Sustainability 2012, 4, 3279–3301. [CrossRef]
33. Zhang, W.; Li, K.; Zhou, D.; Zhang, W.; Gao, H. Decomposition of intensity of energy-related CO2 emission
in Chinese provinces using the LMDI method. Energy Policy 2016, 92, 369–381. [CrossRef]
34. Tan, Z.; Li, L.; Wang, J.; Wang, J. Examining the driving forces for improving China’s CO2 emission intensity
using the decomposing method. Appl. Energy 2011, 88, 4496–4504. [CrossRef]
35. Wang, Z.; Zhang, B.; Liu, T. Empirical analysis on the factors influencing national and regional carbon
intensity in China. Renew. Sustain. Energy Rev. 2016, 55, 34–42. [CrossRef]
36. Meng, X.; Cheng, G.; Zhang, J.; Wang, Y.; Zhou, H. Analyze on the spatialtemporal characteristics of GHG
estimation of livestock’s by life cycle assessment in China. China Environ. Sci. 2014, 34, 2167–2176.
37. Yao, C.; Qian, S.; Li, Z.; Liang, L. Provincial animal husbandry carbon emissions in China and temporal-spatial
evolution mechanism. Resour. Sci. 2017, 39, 698–712.
38. Luo, Y.; Long, X.; Wu, C.; Zhang, J. Decoupling CO2 emissions from economic growth in agricultural sector
across 30 Chinese provinces from 1997 to 2014. J. Clean. Prod. 2017, 159, 220–228. [CrossRef]

63
Sustainability 2018, 10, 2492

39. Tian, Y.; Zhang, J.-b.; He, Y.-y. Research on Spatial-Temporal Characteristics and Driving Factor of
Agricultural Carbon Emissions in China. J. Integr. Agric. 2014, 13, 1393–1403. [CrossRef]
40. Xiong, C.; Yang, D.; Xia, F.; Huo, J. Changes in agricultural carbon emissions and factors that influence
agricultural carbon emissions based on different stages in Xinjiang, China. Sci. Rep. 2016, 6, 36912. [CrossRef]
[PubMed]
41. Tian, J.; Yang, H.; Xiang, P.; Liu, D.; Li, L. Drivers of agricultural carbon emissions in Hunan Province, China.
Environ. Earth Sci. 2016, 75, 1–17. [CrossRef]
42. Xiong, C.; Yang, D.; Huo, J. Spatial-Temporal Characteristics and LMDI-Based Impact Factor Decomposition
of Agricultural Carbon Emissions in Hotan Prefecture, China. Sustainability 2016, 8, 262. [CrossRef]
43. Yao, C.; Qian, S.; Mao, Y.; Li, Z. Decomposition of impacting factors of animal husbandry carbon emissions
change and its spatial differences in China. Trans. Chin. Soc. Agric. Eng. 2017, 33, 10–19.
44. Zhuang, M.; Gongbuzeren, L.W. Greenhouse gas emission of pastoralism is lower than combined
extensive/intensive livestock husbandry: A case study on the Qinghai-Tibet Plateau of China. J. Clean. Prod.
2017, 147, 514–522. [CrossRef]
45. Luo, T.; Yue, Q.; Yan, M.; Cheng, K.; Pan, G. Carbon footprint of China’s livestock system—A case study of
farm survey in Sichuan province, China. J. Clean. Prod. 2015, 102, 136–143. [CrossRef]
46. Xue, B.; Wang, L.Z.; Yan, T. Methane emission inventories for enteric fermentation and manure management
of yak, buffalo and dairy and beef cattle in China from 1988 to 2009. Agric. Ecosyst. Environ. 2014, 195,
202–210. [CrossRef]
47. Xu, X.; Lan, Y. A comparative study on carbon footprints between plant- and animal-based foods in China.
J. Clean. Prod. 2016, 112, 2581–2592. [CrossRef]
48. Wang, L.-Z.; Xue, B.; Yan, T. Greenhouse gas emissions from pig and poultry production sectors in China
from 1960 to 2010. J. Integr. Agric. 2017, 16, 221–228. [CrossRef]
49. Ang, B.W. LMDI decomposition approach: A guide for implementation. Energy Policy 2015, 86, 233–238.
[CrossRef]
50. National Development and Reform Commission of China (NDRCC). Guidelines for the Development of Low
Carbon and Provincial Greenhouse Gas Inventories; NDRCC: Beijing, China, 2013.
51. IPCC. IPCC Guidelines for National Greenhouse Gas Inventories Volume 4: Agriculture, Forestry and Other Land
Use; IPCC: Geneva, Switzerland, 2006.
52. IPCC. Clim. Chang. 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change; Core Writing Team, Pachauri, R.K., Reisinger, A., Eds.;
IPCC: Geneva, Switzerland, 2007.
53. Wang, G.G.; Wang, M.L.; Yang, C. Characteristics and Mechanism of Animal Husbandry’s Geographical
Agglomeration in China. J. Nat. Resour. 2014, 29, 2137–2146.
54. Thornton, P.K. Livestock production: Recent trends, future prospects. Philos. Trans. R. Soc. B Boil. Sci. 2010,
365, 2853–2867. [CrossRef] [PubMed]
55. Herrero, M.; Thornton, P.K. Livestock and global change: Emerging issues for sustainable food systems.
Proc. Natl. Acad. Sci. USA 2013, 110, 20878–20881. [CrossRef] [PubMed]
56. Ren, J. Grassland Science; China Agriculture Press: Beijing, China, 1961.
57. Fu, Q.; Zhu, Y.; Kong, Y.; Sun, J. Spatial analysis and districting of the livestock and poultry breeding in
China. J. Geogr. Sci. 2012, 22, 1079–1100. [CrossRef]
58. Wang, G.; Wang, M.; Wang, J.; Yang, C.; Liu, Y. Characteristics and influencing factors of grass-feeding
livestock breeding in China: An economic geographical perspective. J. Geogr. Sci. 2016, 26, 501–512.
[CrossRef]
59. Key, N.; Tallard, G. Mitigating methane emissions from livestock: A global analysis of sectoral policies.
Clim. Chang. 2011, 112, 387–414. [CrossRef]
60. Wang, W.; Koslowski, F.; Nayak, D.R.; Smith, P.; Saetnan, E.; Ju, X.; Guo, L.; Han, G.; de Perthuis, C.; Lin, E.;
et al. Greenhouse gas mitigation in Chinese agriculture: Distinguishing technical and economic potentials.
Glob. Environ. Chang. 2014, 26, 53–62. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

64
 sustainability

Article
Results from On-The-Ground Efforts to Promote
Sustainable Cattle Ranching in the Brazilian Amazon
Erasmus K.H.J. zu Ermgassen 1, * ID , Melquesedek Pereira de Alcântara 2 , Andrew Balmford 1 ,
Luis Barioni 3 , Francisco Beduschi Neto 4,5 , Murilo M. F. Bettarello 6 , Genivaldo de Brito 7 ,
Gabriel C. Carrero 2,8 , Eduardo de A.S. Florence 4 ID , Edenise Garcia 7 ID ,
Eduardo Trevisan Gonçalves 9 , Casio Trajano da Luz 9 , Giovanni M. Mallman 7 ,
Bernardo B.N. Strassburg 10,11 , Judson F. Valentim 12 ID and Agnieszka Latawiec 10,11,13,14
1 Conservation Science Group, Department of Zoology, University of Cambridge,
David Attenborough Building, Pembroke Street, Cambridge CB2 3EQ, UK; [email protected]
2 Institute for Conservation and Sustainable Development of the Amazon, Rua Barão de Solimões 12,
Manaus, AM 69058-250, Brazil; [email protected] (M.P.d.A.);
[email protected] (G.C.C.)
3 Embrapa Agriculture Informatics, Av. André Tosello, nº 209, Campus da Unicamp, Campinas,
SP 13083-886, Brazil; [email protected]
4 Instituto Centro de Vida, Av. Ariosto da Riva, 3473- St E, Alta Floresta, MT 78580-000, Brazil;
[email protected] (F.B.N.); fl[email protected] (E.d.A.S.F.)
5 Grupo de Trabalho da Pecuária Sustentável, Av. Paulista 1754 -Cj. 146, Bela Vista, SP 01310-920, Brazil
6 Via Verde Consultoria Agropecuária em Sistemas Tropicais, Rua Mariana Amaral 138,
São Sebastião do Paraíso, MG 37950-000, Brazil; [email protected]
7 The Nature Conservancy, Belém, PA 66035-115, Brazil; [email protected] (G.d.B.); [email protected] (E.G.);
[email protected] (G.M.M.)
8 Department of Geography, University of Florida, 3141Turlington Hall, Gainesville, FL 32611-7315, USA
9 Instituto de Manejo e Certificação Florestal e Agrícola, Estrada Chico Mendes 185, Piracicaba,
SP 13426-420, Brazil; eduardo@imaflora.org (E.T.G.); casio@imaflora.org (C.T.d.L.)
10 International Institute for Sustainability, Estrada Dona Castorina 124, Rio de Janeiro, RJ 22460-320, Brazil;
[email protected] (B.B.N.S.); [email protected] (A.L.)
11 Rio Conservation and Sustainability Science Centre, Department of Geography and the Environment,
Pontifical Catholic University of Rio de Janeiro, Rio de Janeiro, RJ 22453-900, Brazil
12 Embrapa Acre. Rodovia BR-364, km 14, Caixa Postal 321., Rio Branco, SC 69908-970, Brazil;
[email protected]
13 School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
14 Institute of Agricultural Engineering and Informatics, Faculty of Production and Power Engineering,
University of Agriculture in Krakow, Balicka 116B, 30-149 Krakow, Poland
* Correspondence: [email protected] or [email protected]; Tel.: +44-01223-765398

Received: 12 March 2018; Accepted: 16 April 2018; Published: 23 April 2018

Abstract: Agriculture in Brazil is booming. Brazil has the world’s second largest cattle herd and is the
second largest producer of soybeans, with the production of beef, soybeans, and bioethanol forecast to
increase further. Questions remain, however, about how Brazil can reconcile increases in agricultural
production with protection of its remaining natural vegetation. While high hopes have been placed on
the potential for intensification of low-productivity cattle ranching to spare land for other agricultural
uses, cattle productivity in the Amazon biome (29% of the Brazilian cattle herd) remains stubbornly
low, and it is not clear how to realize theoretical productivity gains in practice. We provide results from
six initiatives in the Brazilian Amazon, which are successfully improving cattle productivity in beef
and dairy production on more than 500,000 hectares of pastureland, while supporting compliance with
the Brazilian Forest Code. Spread across diverse geographies, and using a wide range of technologies,
participating farms have improved productivity by 30–490%. High-productivity cattle ranching
requires some initial investment (R$1300–6900/ha or US$410–2180/ha), with average pay-back times
of 2.5–8.5 years. We conclude by reflecting on the challenges that must be overcome to scale up

Sustainability 2018, 10, 1301; doi:10.3390/su10041301 65 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 1301

these young initiatives, avoid rebound increases in deforestation, and mainstream sustainable cattle
ranching in the Amazon.

Keywords: livestock; Amazon; beef; dairy; sustainable intensification; land sparing

1. Introduction
There is growing competition for land use in Brazil. Beef, soy, and bioethanol production are
forecast to grow 24%, 39%, and 27%, respectively, in the next decade [1], even as the government
has committed to reforest 12 million hectares of land and reduce deforestation—with zero illegal
deforestation by 2030 [2]. As pasture makes up the majority of agricultural land, high hopes are placed
on the potential for increases in cattle productivity to spare land and accommodate the expansion of
other land uses.
The productivity of Brazilian beef production is currently low; only one-third of its sustainable
potential [3]. Brazil could in theory meet demand for beef, crops, and timber until 2040 without
further conversion of natural ecosystems, by increasing cattle productivity to half of that potential [3].
Since livestock make up 37% of Brazil’s greenhouse gas emissions [4] and extensive cattle ranching has
historically been associated with deforestation, cattle productivity improvements are also key to Brazil’s
climate goals [5]. It is hoped that cattle intensification will reduce greenhouse gas emissions through
land sparing [6], increased soil carbon sequestration [7], and increased greenhouse gas intensity [8].
The Brazilian contribution to the United Nations Framework Convention on Climate Change (UNFCC,
New York, NY, USA), includes commitments to reduce deforestation and increase cattle productivity
through the restoration of 15 million hectares of degraded pasture [2].
In this study, we report the results from six on-the-ground initiatives which have been working to
turn theory into practice by increasing the productivity of cattle ranching in the Brazilian Amazon,
a region with low productivity and high potential [3]. First, we describe the current state of beef and
dairy production in the Brazilian Amazon, before we summarize the results from six initiatives which
are raising cattle productivity in the region. We show that there are many ways for cattle ranching
production to be increased on existing pastureland; these initiatives are diverse in geography and the
technologies adopted, and we summarize common successes and challenges faced by all. We then
finish by reflecting on the risks and mechanisms for achieving wide-scale higher-productivity cattle
ranching in the region.

1.1. Beef Production in the Brazilian Amazon

Nearly one third (29%) of the Brazilian cattle herd, the second largest in the world, is found
in the Amazon biome (Supplementary Material). Beef production in the region is characterized
by extensive, pasture-based systems. Farmers traditionally keep zebu cattle breeds—80% of cattle
are Nelore Bos indicus [9]—and use few chemical inputs (e.g., fertilizers) and little active pasture
management, leading to gradual soil degradation and loss of productivity [10,11]. By some estimates,
40% of pastures are in a moderate or advanced state of degradation [12], and cattle stocking rates are
well below their potential [3], with little increase seen since the early 2000s [13]. These systems are
typically only marginally profitable [14].
The cycle of pasture degradation and low profitability has meant that cattle ranching has
historically been associated with deforestation; pasture makes up 60% of deforested land in the
Legal Amazon region [15]. Recently, beef production and deforestation have uncoupled (Figure 1) and
there is growing acknowledgement of the complex mix of drivers underlying deforestation. From the
mid-2000s onwards, deforestation fell 70% through a combination of improvements in enforcement
on private land [16], expansion of protected areas [17], market-initiatives [18], and an economic
slowdown [19]. As deforestation again creeps upwards [20], debate continues about the relative

66
Sustainability 2018, 10, 1301

importance of beef production, land speculation, and the rapid expansion of cropland as underlying
drivers of deforestation in the Amazon [21–24].

Figure 1. (a) Deforestation fell 70% from the mid-2000s onwards; (b) even as the cattle herd in the
Amazon biome continued to grow. Data from: [25,26].

Finally, Amazonian beef is becoming increasingly integrated into the global economy. Improved
animal health control, such as expanding the zone of eradication of foot-and-mouth disease,
has facilitated a growth in exports [27]. While most beef from the Legal Amazon region is still
consumed domestically, exports have more than doubled from <5% of production in early 2000s to
13.5–17.4% of production by 2011 (Figure S1, Supplementary Material).

1.2. Dairy Production in the Brazilian Amazon

Dairy production in the Amazon is a smaller scale operation than beef ranching. Dairy cattle
make up only 3.9% of all cattle in the Amazon biome [25], which is responsible for 6.3–8.7% of Brazilian
milk production [25]. Dairy farming is dominated by family farms (Figure 2), producing milk for
subsistence or the local market. These farms have up to 70 cattle per farm, with low use of chemical
inputs and a strong reliance on family labor [28,29]. Milk production is pasture-based, with some
farms providing supplementary feed (e.g., sugar cane silage or concentrates) in the dry season or at
the milking parlor.
Dairy productivity is therefore low and can be improved. Most dairy cattle are dual-purpose
zebu breeds, though the use of dairy breeds and cross-breeds is increasing, for example, the number
of registered Gir cattle (a specialized dairy breed) increased 70% (to more than 300,000 cattle) from
2007–2012 [30], though they still make up only a small proportion of the 22 million milked cows in the
country [25]. Amazon municipalities have a median productivity of 689 L/cow/yr, which is lower than
the median for the rest of Brazil (1224 L/cow/yr), and lags behind other international milk producers,
such as New Zealand and the European Union, which produce 3500–4200 and 4000–8000 L/cow/yr,
respectively [25,31,32].

67
Sustainability 2018, 10, 1301

Figure 2. Dairy farming is dominated by family farms, both in terms of (a) the number of properties,
and (b) number of dairy cattle. Data from: [33]. Family farming in Brazil is legally defined by a
maximum farm size (ranging from 20–440 ha, dependent on the region), the number of permanent
employees, and the proportion of non-agricultural income.

2. Materials and Methods

A questionnaire about the financial and production performance of sustainable cattle ranching
initiatives (available in the Supplementary Material) was shared with the representatives of four
organizations (The Nature Conservancy, Instituto Centro da Vida, Embrapa, and Idesam) who attended
a conference on sustainable cattle ranching initiatives in Rio de Janeiro in September 2015. To increase
our sample size, a further three initiatives operating in the Amazon region were then contacted
(either directly or through the Brazilian Roundtable for Sustainable Beef, Portuguese acronym, GTPS);
one of which (Florestas de Valor) provided sufficient data to participate. In total, six initiatives (led by
five organizations) participated, as outlined in Table 1.
Two versions of the survey were circulated, one for beef and one for dairy intensification initiatives,
structured as follows. Questions were grouped into eight sections on the (i) overview of the project
(name of the initiative, and institutions involved); (ii) characteristics of the initiative (the number and
types of farm participating, number of cattle and area of pasture intensified, and the year the initiative
began); (iii) details of the package of technologies implemented on participating farms (farm and
pasture management, forage species, use of supplementary feed, etc.); (iv) the costs involved in the
implementation of improved farm management; (v) the costs involved in maintenance of improved
pasture; (vi) the productivity achieved on the farm, in terms of stocking rates (animal units/ha,
where one animal unit is equivalent to a 450 kg cow), beef production (in arroba/hectare/yr, where
one arroba, abbreviated as “@”, is a common Brazilian livestock unit, equivalent to 15 kg of carcass
deadweight), or milk production (liters of milk per cow and per hectare per year); (vii) details of other
measures of performance (e.g., environmental compliance, greenhouse gas emissions); and (viii) details
of how farmers were recruited to each initiative and the respondent’s reflections on the barriers and
opportunities for improved cattle ranching.
The surveys were completed by project managers and field technicians for each initiative, who are
co-authors of this review. Where survey responses were not clear, they were clarified via email by the
first author. Survey data was complemented with published results from initiatives where available
(e.g., [34–41], and all authors provided substantial revision of the manuscript text to ensure it accurately
describes each intervention.

68
 Table 1. Characteristics of the cattle intensification initiatives surveyed.

Hectares of Mean Farm Forest Code

Lead Beef Most Important Year Number Number
Name of Initiative Location Land under Size, Hectares Compliance
Organization or Dairy Management Features Project Started of Farms of Cattle
Intensification (Range) Required?
Pueraria
Intensification of beef Vegetative planting of phaseoloides
5400 a 480,000 a
cattle production systems mixed legume-grass introduced in
1976; No data No data
with the use of mixed Embrapa State of Acre Beef pastures, persistent NA
Sustainability 2018, 10, 1301

available available
grass-legume pastures legume supply of Arachis pintoi
in Acre symbiotically fixed introduced in 2000 137,600
nitrogen 1999
Alta Floresta,
Pasture rotation, pasture
Nova Canaã do
Novo Campo Program ICV Beef fertilization, application 2012 23 14,300 23,800 200 (30–900) Yes
Norte, Paranaíta e
of GAP
Cotriguaçu (MT)
Pasture rotation, pasture
São Félix do
Do Campo à Mesa TNC Beef fertilization, application 2013 13 20,208 34,043 3077 (100–6900) Yes
Xingu (PA)
of GAP
Pasture rotation,
Silvopastoral system
agroforestry with timber
with rotational grazing Idesam Apuí (AM) Beef 2011 10 236 566 b 570 (53–3020) Yes
and leguminous trees,

69
for beef
improved book-keeping
Pasture rotation,
agroforestry with
Silvopastoral system Apuí, Manicoré,
leguminous trees,
with rotational grazing Idesam Novo Dairy 2014 11 95 332 b 188 (83–340) Yes
improved book-keeping,
fo dairy Aripuanã (AM)
and drinking water
system
Rotational grazing,
São Félix do
Florestas de Valor IMAFLORA Dairy leguminous trees lining 2015 6 50 145 83 (25–200) Yes
Xingu (PA)
fenced plots
a Figures from 2004, the last year that production practices in the region were surveyed; b Estimate based on mean stocking rates and pasture area of farms. Ranges are listed in brackets,

where provided. State abbreviations: Embrapa = the Brazilian Corporation for Agriculture Research; ICV = Instituto Centra da Vida; TNC = The Nature Conservancy; Idesam = Institute
for Conservation and Sustainable Development of the Amazon; IMAFLORA = Institute of Forestry and Agricultural Management and Certification; MT = Mato Grosso; AM = Amazonas;
PA = Pará.
Sustainability 2018, 10, 1301

3. Results
We provide results from six sustainable cattle intensification initiatives in the Amazon biome,
four working with beef producers and two with dairy producers (Table 1). While one of these initiatives
was launched in 1976 and introduced legume pasture technologies which have since been adopted on
more than 5000 farms, the remaining initiatives are more recent (established post-2011). These latter
initiatives operate on 63 farms raising 59,000 cattle on 35,000 hectares of pasture in three states (Figure 3).
The technologies deployed are diverse, ranging from relatively low-input leguminous systems to more
input-intensive rotational grazing systems.

Figure 3. Map of Brazil, with the Amazon biome colored in green, and the municipalities where the
sustainable cattle initiatives reported in this article are present shown in other colors.

Each initiative has achieved higher farm productivity, boosting meat production per hectare by
30–270% and dairy production per hectare up to 490% (Tables 2 and 3). While the use of higher-yielding
technologies is profitable in most cases, it requires initial investment to improve farm productivity,
with payback times ranging from 1.5–12 years. The specifics and results of each initiative are described
in more detail below.

3.1. Beef Case Study #1—Intensification of Cattle Production Systems with the Use of Mixed Grass-Legume
Pastures in Acre
In 1976, the Brazilian Corporation for Agriculture Research (Embrapa, Brasília, Brazil) established
the Program for Reclamation, Improvement and Management of Pastures in the Brazilian Amazon
(PROPASTO) which included a series of on-farm experiments to promote the adoption of mixed
legume pastures in the state of Acre [40]. A number of cultivars were launched, of which one legume,
Pueraria phaseoloides (tropical kudzu), was the first to be adopted at scale. By 2004, tropical kudzu was
present in over 30% (480,000 ha) of the total pasture area in Acre and has been successfully planted in
combination with a variety of grass species (Table S1, Supplementary Material) [40].

70
 Table 2. Productivity and profitability of initiatives increasing productivity of beef production. Ranges listed in brackets, where provided.

Increase in
Baseline Baseline Average Years to Break Years to Typical Profit/
Stocking Stocking Productivity Additional
Name of Initiative Stocking Rate Productivity Increase in Even on Achieve Max Hectare/Year
Rate (AU/ha) Rate over (@/ha/yr) References
(AU/ha) (@/ha/yr) Productivity Investment Productivity (R$)
Baseline
Mixed
Intensification of grass-Pueraria
beef cattle 1.5 (1–2) 1.5x 10 (4.9–12.5) 1.3x 3 (2–4) 2 (1.5–3) 149–271
phaseoloides
Sustainability 2018, 10, 1301

production pastures 1* 8 (4–10) * [39,42–

systems with the
Mixed 44]
use of mixed
grass-legume grass-Arachis 2.2 (1.5–3.59) 2.2x 12 (13–35) 1.5x 4 (3–5) 3 (2–5) 296–381
pastures in Acre pintoi pastures
Novo Data not
1.22 * 2.8 (1.5–3.5) 2.3x 4.7 * 10.8 (7–27) 2.1x 2.5 (1.5–4) 602 (173–1140) [4,38]
Campo Program provided
1.06 5.87
Do Campo à Mesa 0.87 (0–2.81) 1.2x 4.5 (0.9–10.5) 1.3x 8.5 (7–12) ~6 432 (−546–1103) [37]
(0.27–3.05) (1.42–19.2)
Silvopastoral
System with
0.60 (0.45–0.7) 2.4 (2.0–2.7) 4.0x 5.5 (4–7) 15 (12–20) 2.7x 5 (4–6) 5 ~263 -
Rotational Grazing
for Beef
AU = animal stocking unit, equivalent to a 450 kg cow; @ = 15 kg of carcass (deadweight). * productivity data are not available from participating farms pre-adoption, and so the baseline

71
data are estimates of the regional average productivity without the adopted technology. Estimates of profitability do not include revenues from farm activities not directly related
with cattle production (e.g., sale of timber trees or crops), and costs are representative of the interventions made on participating farms (they do not, for example, consider the cost of
acquiring land or purchasing cattle, as participating farms used on-farm resources for intensification).
Sustainability 2018, 10, 1301

Embrapa began by introducing mixed legume pastures on properties belonging to three farmers,
who were identified as innovators [40]. Knowledge of these novel technologies then spread through
word of mouth and trained agricultural extension officers. Legumes were promoted because of their
ability to fix nitrogen, which reduces pasture maintenance costs and produces a protein-rich sward
(Figure 4); a pasture sown with 20–45% Tropical kudzu produces nitrogen equivalent to approximately
60–120 kg of N/ha/yr [42]. Grass-legume associations cost between R$1350–2000/hectare to
implement, and around R$100/ha/yr to maintain (Table 4) and are therefore a relatively low-cost
intensification technology for pasture restoration and intensification. Tropical kudzu pastures produce
modest productivity improvements, supporting 1.5 animal units/ha and producing 4.9–12.5 @/ha/yr
(Table 2).

Figure 4. Leguminous pasture plants (above the dashed line) have higher protein content than
conventional grasses (below dashed line). Source: [45].

Since a peak in the early 2000s, the popularity of Tropical kudzu has declined as it showed
poor compatibility with some of the newer grass species being planted by farmers, such as African
stargrass (Cynodon nlemfuensis), and also failed to persist when managed in more intensive production
systems using mixed pastures with other grasses and rotational grazing at stocking rates above
1.5 animal units per hectare. For these situations, Embrapa promoted forage peanut cultivar Belomonte
(Arachis pintoi) [41].
This new cultivar was released in 1999 in Bahia, Brazil. First planted by a single farmer in Acre in
2000, in April 2001 20 farmers planted this legume together with a variety of grasses (Figure 5 and
Table S1, Supplementary Material). Adoption was rapid. By March 2004, close to 1000 small, medium
and large farmers of Acre had already introduced forage peanut into 65,000 ha of pasture [41], and by
2015 forage peanut was planted across 2000 farms and 137,000 ha in Acre [39], approximately nine
percent of the state’s pasture area [46].
Forage peanut can be either planted along with other grasses during pasture restoration
(i.e., replanting of a degraded pasture), or introduced onto existent pasture during the rainy season.
Since forage peanut cultivar Belomonte does not produce seeds (it instead reproduces vegetatively),
it must be planted using stolon cuttings. Farmers usually set aside an area (<1 ha) where forage peanut
grows in dense stands (i.e., without competing grasses), from which the vegetative stolons are then
harvested for planting in pasture. Embrapa have successfully developed a number of techniques for
establishing grass-legume pastures using vegetative propagation of forage peanut and stoloniferous
grasses, depending on the farmer’s technology level, ranging from semi- to fully-mechanized and
either conventional or no-till agriculture [34]. African stargrass-forage peanut pastures managed under
rotational grazing can support up to 3 animal units/ha (Table 2), producing Nelore × Angus crossbred

72
Sustainability 2018, 10, 1301

steers ready for slaughter within 24 months (Table S2, Supplementary Material), compared with the
36+ months typical of extensive systems [41]. These productivity improvements also improve the
farm bottom line, increasing profitability from around R$41.10/ha/yr in traditional systems up to
R$381.28/ha/yr (Table 2).

Figure 5. Nelore cattle (Bos indicus) grazing mixed pasture: forage peanut (Arachis pintoi cv.
Belomonte) (the yellow flowering plants) with Brachiara spp.

Grass-legume pastures can mitigate greenhouse gas emissions by substituting for fossil-fuel
dependent nitrogen fertilizers, by reducing cattle slaughter ages [42,47], and by increasing soil carbon
sequestration [48]. Additionally, Costa et al. [49] reported that mixed pastures of Brachiaria humidicola and
forage peanut cv. Mandobi in Acre had 24% lower N2 O emission (2.38 kg N ha−1 yr−1 ) than pure pasture
of the same grass (3.13 kg N ha−1 yr−1 ) and similar emissions to native forest (2.47 kg N ha−1 yr−1 ).

3.2. Beef Case Study #2—Novo Campo Program

The Novo Campo Program (“New Field” Program in English) has involved 23 farms in the Alta
Floresta region of Mato Grosso since 2012. Led by the Instituto Centro de Vida (ICV), with collaboration
with stakeholders from across the cattle supply chain (see Table 4 for a complete list of participating
organizations), cattle productivity has been increased through a package of farm management changes.
These include the introduction of pasture rotation, the adoption of so called “good agricultural
practices” (GAP), correction of soil imbalances (e.g., by liming), pasture fertilization, and improved
farm record keeping. The GAP is a voluntary set of “gold-standard” guidelines for sustainable
production adopted across Brazil, which includes a check-list of 125 points of guidance across 11 areas
of farm management, spanning farm economic management, social and environmental responsibilities,
to pasture and herd management [50].
Together, these interventions have improved farm productivity and profitability, and reduced
greenhouse gas emissions (Figure 6). Beef production per hectare has increased from ~4.7 (the regional
average) to 7–24 @/ha/yr, which has reduced the cost of production per arroba on intensified farms by
one third (R$66.33/@ vs. R$95.80/@) [38]. Profit increased from less than R$100/ha/yr to more than
R$600/ha/yr of pasture (Table 2). These yield-raising technologies require an initial investment of
R$1500–4000/ha, depending on the initial pasture condition, though these up-front costs are paid off
after an average of 2.5 years (Table 2).

73
 Table 3. Productivity of dairy intensification initiatives surveyed. Ranges are listed in brackets, where provided.

Baseline Increase in Increase in Increase in Years to

Stocking Baseline Baseline Years to Break
Stocking Stocking Productivity Productivity Productivity Productivity Achieve Typical
Name of Initiative Rate Productivity Productivity Even on
Rate Rate over (L/ha/yr) Over (L/cow/yr) over Max profit/ha/yr (R$)
(AU/ha) (L/ha/yr) (L/cow/yr) Investment
(AU/ha) Baseline Baseline Baseline Productivity
Silvopastoral System
0.75 3.5 5794 1551 1954
with Rotational 4.7x ~1192 4.9x 1.26x 2.6 (1.8–6.8) 6 (5–7) 4425 (2176–8092)
(0.5–1.08) (2.4–6.3) (2969–9037) (760–1825) (1642–2482)
Grazing for Dairy
Sustainability 2018, 10, 1301

3.1 Data not Data not Data not

Florestas de Valor 1.1 (0.9–1.2) * 2.8x ~3190 ~760 ~1100 1.4x 4 (3–5) 3 (2–4)
(2.5–3.7) provided provided provided
* productivity data are not available from participating farms pre-adoption, and so the baseline data are estimates of the regional average productivity without the adopted technology.

Table 4. Typical costs involved in each intensification initiative. Degraded pastures are pastures with declining pasture fertility; their restoration often requires soil
correction, ploughing, and reseeding of grasses, whereas soil correction and ploughing may not be required for conventional pasture improvement. Ranges are
listed in brackets, where provided.

Cost of Intensification (R$/ha) Cost of Pasture Cost of

Name of Initiative Organizations Involved Ranching Systems Improvement Improvement of Maintenance Technical
of Degraded Conventional (R$/ha/yr) Assistance
Pasture Pasture (R$/property/yr)

74
Semi-mechanized conventional
Intensification of beef cattle Embrapa Acre, Federação de Agricultura do Estado do planting: 2011.
production systems with the AcreFundo de Desenvolvimento da Pecuária do Estado Cow-calf, calf raising & Mechanized conventional planting: Data not
~100
use of mixed grass-legume do Acre, & Associação para o Fomento à Pesquisa de fattening, full cycle 1461–1920. collected
pastures in Acre Melhoramento de Forrageiras Mechanized no-till planting:
1347–1806
ICV, International Institute for Sustainability (IIS),
Embrapa, Solidariedad, Sindicatos Rurais de Alta
3500 8000
Novo Campo Program Floresta e Cotriguaçu, JBS, McDonalds, Arcos Calf raising & fattening 2000 (1500–2000) 1800 (1500–2000)
(3000–4000) (6000–12000)
Dourados, IMAFLORA, Althelia Ecosphere, Terras,
GTPS, Fundo Vale, Norad, & the Moore Foundation
1890 Data not
Do Campo à Mesa TNC, Marfrig, Walmart, GTPS, & the Moore foundation Calf raising & fattening 1468 (1318–1571) ~680
(1750–1897) collected
Idesam, Centro para Investigación en Sistemas
Silvopastoral System with Sostenibles de Producción Agropecuária (CIPAV), Via Cow-calf, calf raising 2666 All farms had
~216.25 ~5480
Rotational Grazing for Beef Verde Consultoria Agropecuária, Fundo Vale, & Viveiro & fattening (2412–3021) degraded pasture
Santa Luzia
Silvopastoral System with Idesam, CIPAV, & Via Verde Consultoria Agropecuária, 5355 All farms had
Cow-calf ~275 ~5480
Rotational Grazing for Dairy Fundo Vale, & Viveiro Santa Luzia (4900–6866) degraded pasture
IMAFLORA, CAMPPAX (Cooperativa Alternativa
Mista do Alto Xingu), ADAFAX (Associação
All farms had
Florestas de Valor Desenvolvimento da Agricultura Familiar do Alto Cow-calf ~2500 2000 (1200–2560) 2500 (2000–3000)
degraded pasture
Xingu), CFA (Casa Familiar Rural de São Felix do
Xingu), Petrobras, Fundo Vale, & Fundo Amazônia
Sustainability 2018, 10, 1301

By improving animal growth rates and so achieving slaughter weight in fewer days, farmers
reduce emissions from enteric fermentation across the animal’s lifetime (enteric fermentation
contributes 67–83% of emissions, excluding land use change—a topic we return to in Section 4 [8,51,52]).
This is seen from the experience on Novo Campo Program farms. Emissions have been reduced by
36–59% (Figure 6), in large part through reductions in slaughter age down to 20–24 months (Table S2,
Supplementary Material).

Figure 6. Two estimates for the emissions per kilogram of beef of conventional ranches and Novo
Campo Program farms. Piatto and Costa Junior [53] compare emissions on pilot farms before
pasture intensification (baseline), with emissions after two years of participating in the initiative.
Bogaerts et al. [8] compare farms participating in the Novo Campo Program with neighboring
non-participating farms. While both studies include emissions from enteric fermentation, manure
management, pasture fertilization, and fossil fuels required for pasture restoration, Bogaerts et al.
also include emissions from concentrate feed production, and Piatto and Costa Junior include carbon
sequestration in improved pasture and soil carbon emissions from degraded pasture. No emissions
from land use change are included, because no recent deforestation occurred on sampled farms.

Key changes in farm management are improved book-keeping and the introduction of rotational
pasture management. Adequate book-keeping is fundamental to understanding and improving farm
management processes, and yet is not done by a majority of farm managers or owners [4]. Farmers are
therefore trained in the importance of recording the costs of all inputs and the quantity and value of
beef produced, to allow the calculation of the income and profit per arroba of beef. Once the economic
performance of the farm is established, rotational grazing is introduced.
Typically, 10–30% of the farms’ pasture area is fenced off into ca. 5-hectare plots, which are
targeted for pasture improvement. Pasture restoration begins with soil analysis to identify soil
imbalances (e.g., pH). The pasture is then ploughed and limed (typically with 1500 kg/ha lime; Table S3,
Supplementary Material), and the pasture is fertilized (400 kg/ha) and replanted, with Panicum
maximun cv. Mombaça or Panicum maximun cv. Tanzânia grasses (Figure 7).
These fertilized plots have much higher productivity than conventionally managed pasture;
in the first two years of the project, they produced 20.75 @/ha/yr compared with 10.75 @/ha/yr
across the farm as a whole (Marcuzzo and de Lima, 2015). Cattle are moved through each fenced plot
sequentially; the stocking rate and exact timing of the cattle rotation are based on the season, forage
height, and planted species, manipulated to maximize cattle growth while maintaining pasture fertility.
With Panicum maximun cv. Mombaça, cattle enter plots when the grass height is around 90 cm and
are moved when it has been grazed down to around 40 cm (approximately every five days in the wet
season, and less frequently during the dry season).

75
Sustainability 2018, 10, 1301

Figure 7. (a) High-yielding cattle pasture (right) on a Novo Campo Program farm, one month after
replanting, compared with conventional, unreformed pasture (left); (b) Stocking rate in intensified
pasture plots for the period January 2013–September 2014. The grey dashed line represents the mean
stocking rate for farms in the region. Adapted from: [38].

While forage is in abundant supply in the rainy season (from approximately December–May), in the
dry period, stocking rates in the intensified pasture areas are reduced (Figure 7), and supplementary
feeding is necessary. Novo Campo Program farms have adopted a semi-feedlot feeding approach,
where cattle are given supplementary concentrate feed in troughs in a confined area of pasture.
One farm has also integrated soy and beef production to boost dry season feed availability. Soy is
planted on 200 ha, which is seeded with Brachiaria spp. after the soy harvest. This additional pasture
area then serves as an additional forage source during the dry period.
All Novo Campo participating farmers qualify for the GAP certificate, developed by Embrapa.
The adoption of GAP requires training of farm personnel, and ultimately, approximately a 50% increase
in on-farm labor. To support the dissemination of knowledge to staff on Novo Campo farms and
beyond, ICV therefore linked up with a local university, UNEMAT Alta Floresta, to train an additional
40 agricultural extension officers in GAP, environmental licensing, farm financial analysis, and the use
of farm management software [38].
Farms participating in the Novo Campo Program must also comply with Brazilian National Law
No. 12.651, the so called ‘Forest Code’. They must be registered in the rural environmental registry
(Portuguese acronym CAR), cannot be blacklisted by the environmental police (IBAMA), and must
have had no illegal deforestation post-2008. On joining the Novo Campo Program, many farms had
degraded riparian areas, which legally must be reforested within 20 years. Properties received support
from ICV in restoring these areas, with the restoration actions depending on the degradation status
and location of streams. Where streams had some secondary regrowth and/or nearby forest, this might
include only fencing-off streams from cattle to foster natural regeneration; where riparian areas were
more degraded or isolated, they may have required direct seeding of trees, removal of grasses and the
control of pests. In both cases, restoration is not cheap with costs varying from R$2360/ha for passive
restoration, to R$9654/ha for active replanting [54].

76
Sustainability 2018, 10, 1301

To scale-up the results achieved in the Novo Campo Program, a commercial spin-off, PECSA,
was launched in 2015. While management of the Novo Campo continues under ICV, PECSA applies
the same package of technologies, in some cases intensifying more than the 30% of pasture area used
in the Novo Campo Program to increase farm productivity 3–5 times above the regional average [55].

3.3. Beef Case Study #3 Do Campo à Mesa

Launched in 2013, as a collaboration between The Nature Conservancy (TNC) and several partners
along the beef supply chain (Table 4), the do Campo à Mesa initiative (“From Field to Table” in English)
operates on 13 farms in São Félix do Xingu, Pará, to boost productivity through the establishment of
rotational pasture and training in GAP. Results after one year of the project are promising; stocking
rates increased 20% and beef productivity 30% (Table 2), with substantially greater gains expected;
beef productivity is forecast to increase more than 3.5-times to 17@/ha (10–27@/ha) within 12 years of
the start of the project [37].
On joining the initiative, baseline data were collected by agricultural extension officers on the
herd structure (e.g., number of animals, category, age, weight), farm operating costs, and soil condition.
These are complemented with remote sensing analyses of the farm’s land use. Many farms had
considerable areas of degraded pasture, 23% and 18% of pasture was moderately or highly-degraded,
respectively [37]. To combat this, management plans were drawn up to improve 20% of the farm’s
pasture area each year so that after five years all pasture would be in improved condition.
Goals for stocking rates were set, aiming to gradually increase stocking rates from 0.87 AU/ha
to 3.0 AU/ha. To achieve this, the initiative has used pasture improvement (weeding and liming,
and resowing of pasture if degraded), education of farm workers in GAP, and the establishment of
rotational grazing. Livestock are also given 1.5 kg/head/day of protein supplementary feed in the dry
season, to overcome the seasonal deficit in feed availability.
The main costs of improving farming practices come in three forms: pasture improvement and
maintenance, adoption of GAP, and costs of environmental compliance; these costs vary strongly with
farm size. Pasture improvement requires an initial investment of between R$1300–1900/ha/yr (Table 4),
and adoption of GAP requires not only worker education, but also improvements in infrastructure
and more farm labor. After 12 years of the project, the requirement for labor is forecast to increase on
average 54%, with larger increases on the biggest farms [37]. On small farms labor is family-based
and will be kept constant, while large farms plan to increase their number of employees three-fold.
Do Campo à Mesa farms must also be compliant with the Forest Code, which also incurs substantial
costs. Compulsory restoration of deforested areas added an extra 30–250% to the cost of adopting
improved farm practices [37]. Taking all the costs of the transition to more sustainable farming practices
together, pasture intensification and legal compliance generated better economic returns for large
farms (>500 ha of pasture) ([37]. Costs per hectare for the three smallest properties were on average
2.3 times higher than for other farms, and the two smallest farms, with 44 and 126 ha of pasture area,
were not projected to make a profit and subsequently elected not to continue with cattle intensification.
To help overcome the initial cost barrier and support the growth of the program, TNC helps farmers
apply for loans from the Brazilian government’s low carbon fund (the “Plano ABC”, in Portuguese).

3.4. Beef Case Study #4—Silvopastoral System with Rotational Grazing for Beef
In 2011, the Institute for Conservation and Sustainable Development of the Amazon (Portuguese
acronym, Idesam) launched the Silvopastoral System with Rotational Grazing initiative (“Sistema
Silvipastoril com Pastejo Rotacional”, in Portuguese), on beef and dairy farms in Apuí, Amazonas.
The initiative is working with 10 beef farms to boost productivity of smallholder beef production
(results for dairy farms are listed in diary case study #1). While the planting of trees and shrubs,
involves high up-front costs (Table 4), participating beef farms have improved productivity from
4–7@/ha/yr to 12–20@/ha/yr, and profitability from ~R$130/ha/yr to R$260/ha/yr (Table 2).

77
Sustainability 2018, 10, 1301

Farm improvement begins with a visit from an agricultural extension technician, collecting
baseline farm information and drawing up management plans with the farmer. To introduce
rotational grazing, an area of between 20–50 hectares is intensified on each farm by restoring pasture
through the application of lime, where required. This area is then divided into six plots, sown with
Panicum maximum cv. Mombaça or Brachiaria brizantha, fertilized with phosphorus, and managed in a
rotational system. Cattle are moved through each plot approximately every 6–7 days according to the
pasture condition.
These plots are divided by double electric fences (1.5 to 2 m in width) protecting a line of trees
planted 3 m apart (Figure 8). The trees are mostly native species, half of which are planted for their
timber or other economic value and the other half are a mix of leguminous tree species (20–30 trees/ha),
including Inga-de-metro (Inga edulis Mart.) Leucaena (Leucaena leucocephala var. cunningham) Paricá
(Schizolobium amazonicum) Gliricídia (Gliricidia sepium), Jatobá (Hymenaea courbaril), and Parkia spp.
Among the trees, fodder shrubs are also planted, including Tithonia diversifolia and Cratília (Cratylia
argentea). The principal benefits of planting leguminous trees and fodder shrubs in pasture are that
the leaves provide a high-protein feed [56], increased shade which can reduce heat stress in cattle [57],
and nitrogen-fixation which boosts grass growth and can improve soil condition [58].

Figure 8. (a) Producer standing with a tree line of 4-month old leguminous trees in an Idesam
silvopastoral system; (b) silvopastoral system once the bushes and trees are 2 years old.

Silvopastoral systems do, however, require careful management and substantial initial investment.
Trees need protection from heavy grazing for the first 12–24 months post-planting; thereafter they
require occasional pruning if they get too broad in order to avoid excessive shade hindering grass
growth [59]. Farmers must also closely monitor herd performance, including daily recording of
stocking rates. These changes require on average a 20% increase in on-farm labor. Farmers are
supported throughout the process by monthly visits from Idesam’s agricultural extension staff.
Costs of implementing silvopastoral systems are high, R$2400–3020/ha, though this is offset by
low maintenance costs around R$220/ha/yr, in part because leguminous pastures do not require any
nitrogen fertilizer application.
While it is hoped that productivity increases will reduce greenhouse gas emissions on participating
farms, a recent analysis found that participating farms had higher greenhouse gas emissions than
neighboring farms (47 vs. 40 kg CO2 e/kg beef) [8]. These results should, however, be treated with
caution as the analysis used the Cool Farm Tool, an out-of-the-box greenhouse gas calculator which
is not tailored for measuring emissions from integrated systems, and the input data were collected
less than one year after the program’s implementation. The environmental and economic impacts of
integrated systems, such as silvopastoral systems, are difficult to model because the different parts of
the management system interact [60], in this case, leguminous trees fertilize the pasture, supporting
grass growth. The Cool Farm Tool, though comprehensive in many respects, does not consider these
interactions, simplifying the farm’s environmental footprint and potentially over-estimating emissions.

78
Sustainability 2018, 10, 1301

Similarly, while the Cool Farm Tool can calculate carbon sequestered in trees on-farm, this source
of sequestration was not included in Bogaerts et al. [8]. Additionally, the farm-level data used were
collected shortly after the implementation of rotational grazing, therefore, emissions associated with
pasture improvement were counted before productivity gains had been realized. As it is expected to
take five years for the systems to achieve full productivity (Table 2), using data from only the first year
overestimates emissions from participating farms.
Finally, to participate in the initiative, farms must also be compliant with environmental legislation.
They must be registered on the CAR, develop a PRAD (the “Projeto de Recomposição de Áreas
Degradadas e/ou Alteradas”, a plan for restoration if the property does not meet minimum legal
requirements for forest cover), and agree to not clear any new areas of forest.

3.5. Dairy Case Study #1—Silvopastoral System with Rotational Grazing for Dairy
Idesam also work with 11 smallholder pilot farms (ranging from 83–340 ha in size; Table 1) in
the state of Amazonas, to increase dairy productivity through the rotational management of pasture
lined with timber and leguminous trees, and shrubs. As for Idesam’s beef intensification in the region,
the dairy initiative has seen productivity improvements, a 1.26-fold increase in milk production per
cow and 4.9-fold increase in milk production per hectare (Table 3).
Plots of intensively managed pasture are divided by doubled electric fences protecting a line
of trees and shrubs. Compared with Idesam’s beef system, the dairy farms use a greater number of
plots (~40) and trees (50 to 110/ha). Around 6 hectares is targeted for intensive management on each
farm, with 0.1 to 0.9 hectares per plot. Forty-four percent of the tree species were planted to provide
shade for cattle and timber as a source of long-term income for farmers; 56% were leguminous [61].
As often required in the region, the soil was supplemented with lime, before planting Brachiaria
brizantha, Panicum maximum cv. BRS zuri or cv. Massai grasses, with phosphorus added as necessary.
These grasses show high productivity in the shady conditions typical of silvopastoral systems [57,62].
Laboratory experiments have shown, for example, that shade can even increase the protein content of
Panicum maximum grasses [63].
The system is managed in rotation, where cattle are moved through plots every 12 h to two days,
depending on grass height. In the drier months, the deep-rooted leguminous trees continue to provide
a source of fodder, and some farmers supplement feed with maize silage or “cut-and-carry” feeding of
Tithonia diversifolia, Inga edulis, and Cratylia argentea. Lactating cattle on some farms also receive 1.5 kg
of maize-based concentrate feed at milking each day. Water availability is crucial for high-productivity
dairy production, and so drinking water is pumped into elevated water boxes, which distribute it by
gravity through a system of buried hoses to each pasture plot (Figure 9).

Figure 9. (a) Installation of underground piping to deliver water to each plot in the Silvopastoral
System with Rotational Grazing for Dairy initiative; (b) Dairy cattle drinking from one of the water
troughs, with electric fencing in the foreground.

79
Sustainability 2018, 10, 1301

Systems with leguminous trees require approximately 15% more labor than conventional
pasture-based systems. The trees require protection from grazing and insects for the first few months,
as well as intermittent pruning during the first three years. The requirement for tree care reduces as the
trees mature, and the rotational management of cattle in these systems requires no additional specific
management, as cattle are moved twice a day for milking in any case.
The implementation of leguminous systems can be costly, ranging from R$4900–6900/ha to cover
the costs of pasture reformation, tree planting, electric fencing (for managing rotational grazing),
and construction of water sources in each plot (Table S3, Supplementary Material). Though these
initial costs are paid off within 2–7 years (Table 3), as improved management boosts profitability from
R$1281.15/ha/yr to around R$4425/ha/yr, Idesam has provided financial support to the first farmers
of the program. Farmers paid 20% of the cost of implementation, with Idesam covering the remaining
80%. To access this financial support and participate in the initiative, farmers must commit to legal
compliance with the Forest Code. Farms must be registered in the CAR, commit to not deforest further,
and restore non-forested areas and degraded riparian strips, in line with the PRAD.

3.6. Dairy Case Study #2—Florestas de Valor

The dairy intensification project Florestas de Valor (“Forests of Value” in English) was launched
by the Institute of Forestry and Agricultural Management and Certification (Portuguese acronym,
IMAFLORA) in 2015, and operates on six farms in São Félix do Xingu in the state of Pará.
By concentrating production on a small, intensively managed portion of pasture in each farm, they have
increased stocking rates almost three-times above the regional average, with 85% higher productivity
per cow (3240 L milk/cow/yr vs. 1750 L/cow/yr; Table 3).
Florestas de Valor operates on small properties, ranging from 25–200 hectares in size (Table 1).
These farms rely almost entirely on family labor, and so it is important that the intensification does not
increase the overall requirement for labor. This is achieved by focusing production on a small area in
each farm, where 3.5–11 hectares are selected for intensification and divided into 10–15 fenced plots
(Figure 10). The soil in each plot is analyzed before soil correction, and either direct resowing with
Brachiaria brizantha MG5, Panicum maximum cv. Mombaça, Brachiaria decumbens or Panicum maximum
cv. Massai, or pasture restoration through crop-livestock integration. On four properties, maize
was planted on degraded pasture; once the maize was harvested, pasture grasses were then sown.
The fences between pasture plots are planted with leguminous trees, including Canavalia ensiformis,
Inga edulis and Cajanus cajan. Trees were planted three meters apart, with an average of 66 trees per
hectare. Cattle remain approximately three days in each plot, thereby completing a cycle of each
plot every 30–45 days. In the dry season, when grass growth is slower and over-grazing is more
likely, less time is spent in the fenced plots, and cattle are instead put onto pasture that has been
intentionally rested.
Overall, it costs around R$2500/ha to implement the rotational grazing and leguminous tree
systems. These costs stem from costs of soil improvement, grass seeds, maize planting, fencing,
solar panels, and in-pasture water sources (Table S3, Supplementary Material). Of the 50 hectares
intensified, IMAFLORA funded 36 hectares, with farmers covering the costs of the remaining
14 hectares. In either case, because of improvements in productivity, the total initial cost is expected to
be paid off within 3–5 years.

80
Sustainability 2018, 10, 1301


Figure 10. Around 10% of each property in the Florestas de Valor initiative is divided into small plots
using fences lined with leguminous trees (yellow lines in the main image). Top right: intensified pasture
area shown within the total farm boundary (black line). Lower right: The farm location is shown
as a point within Sao Felix do Xingu (municipality colored in blue). State abbreviations: PA = Pará,
MT = Mato Grosso, TO = Tocantins.

4. Discussion
The results from these initiatives suggest that there are a variety of available technologies that can
increase cattle ranching productivity and profitability in the Amazon. Though diverse in the details,
these initiatives share many similarities, including their focus on farmer training, farm record-keeping,
and improved pasture management, in particular, the adoption of rotational grazing and pasture
fertilization using chemical inputs or leguminous plants. These management changes require some
initial investment (R$1300–6900/hectare), which is paid off within 2.5–8.5 years.
With the exception of the introduction of grass-legume pastures in Acre, the initiatives presented
are young and further productivity gains are expected, with productivity expected to peak 1.5–7 years
after implementation (Tables 2 and 3). Our study is, however, not a large-scale randomized controlled
trial, and so these promising results come with a number of caveats. First, we do not claim that
our review is exhaustive, though we present results from six of the thirteen initiatives that we
are aware of which operate in the region (Table S4, Supplementary Material), and we believe our
results are broadly representative of high-yielding cattle ranching in the Amazon. Second, these
initiatives recruited farmers opportunistically, predominantly through farmer networks and open
farm days (Figure 11). The farmers participating are therefore “early-adopters”, who may differ
from other farmers in systematic ways, for example by being less risk averse. We do not believe
that the productivity gains that we observe result from these farmer differences or fundamental
differences between these farms and their neighbors. For three of our six initiatives, we present
productivity estimates from before and after the interventions showing clear productivity increases
(for the other three, the Novo Campo Program, Florestas de Valor and mixed legume pastures in Acre,
pre-intervention data were not available and our baseline data are estimates of the regional average
productivity; Tables 2 and 3). Our data are also self-reported, though our productivity improvements
are in line with previous literature on the productivity gains from improvements in farm management
in Brazil [5,64–67], and our estimates of the costs of intensification are an important resource for
accurately estimating the cost-effectiveness of cattle intensification in the Amazon. Previous work on

81
Sustainability 2018, 10, 1301

the cost of cattle intensification has typically focused only on direct costs of pasture improvement,
thereby underestimating the true cost of intensification for farmers. When modelling the pasture
improvement included in Brazil’s contribution to the UNFCC, De Oliveira Silva et al. [5], for example,
estimate costs between R$365–1243/ha and maintenance costs from R$6.9–266.8/ha, estimates which
are substantially lower than our figures. Their figures, however, do not include indirect costs such as
costs from the transportation of inputs, increased labor, or costs from fencing and the implementation
of rotational grazing.

Figure 11. Relative importance (1 = least important, 6 = most important) of six different channels
for recruiting farmers into the six initiatives described in this article. All initiatives recruited
farmers opportunistically, as knowledge about the initiatives was spread for the most part through
word-of-mouth, field days where neighboring farmers were invited to tour participating farms, and the
training of rural extension officers in GAP. Idesam’s beef and dairy initiatives took similar approaches
to recruitment, and so the results are grouped for these two initiatives.

4.1. Risks of Cattle Intensification

Whatever the financial costs, increasing cattle ranching yields in the Amazon is not without
risks [68]. Improving productivity can reduce greenhouse gas emissions from beef production, as seen
both at the farm-scale in the Novo Campo Program (Figure 6) and other intensification initiatives
in the region [8], and at the national-scale from coupled economic-environmental modelling [6].
Cohn et al. [6] find that the adoption of GAP in Brazil could halve greenhouse gas emissions from
deforestation and agriculture, though in practice the land sparing effect of cattle productivity
increases are likely to vary spatially. While in consolidated regions, economic theory suggests that
intensification can help reduce deforestation through market and labor effects [69,70], in forested
regions intensification risks rebound effects—the so-called “Jevon’s paradox” where increases in the
profitability of cattle ranching incentivize, rather than reduce, local deforestation. Reconciling targets
for increased cattle production and zero illegal deforestation or even deforestation-free production will
therefore require explicitly linking improvements in cattle ranching with habitat protection and efforts
to reduce leakage in cattle supply chains [71,72]. It is also with this rebound effect in mind that the
initiatives described in this article explicitly require participating farmers to comply with the Brazilian

82
Sustainability 2018, 10, 1301

Forest Code, have no recent illegal deforestation, and develop land use plans for reforestation where
required. Further discussion of potential risks is included in the online Supplementary Material.
While the technologies discussed in this article can increase farm profitability, this is also not
always the case; results from two of our initiatives show that pasture intensification may, in some
cases, be more profitable on large, rather than small farms. In the do Campo à Mesa initiative, pasture
intensification was not profitable within twelve years for the two smallest farms, suggesting that there
is a tipping point in economic returns between 126 and 425 ha of pasture [37]. Similar economies of
scale were found in a modelling study using data from the Novo Campo Program (which found that the
introduction of GAP and rotational grazing intensification was only profitable on farms with >385 ha
of pasture; IIS, 2015), and in other studies of cattle ranching economics [4,73]. On the other hand,
these economies of scale appear to be technology and system dependent. Positive economic returns
were seen for smallholder dairy producers, and silvopastoral beef systems in Apuí (Tables 2 and 3),
which can turn a profit with as little as 20 hectares of pasture. Similarly, grass-legume pastures
have been adopted by small- and large-farms alike in Acre [41,74]. Given that 78% of cattle-rearing
farms (hosting 33% of cattle) in the Amazon biome have less than 200 hectares of pasture (Figure S2,
Supplementary Material), it is important that efforts to improve profitability and farmer livelihoods in
the cattle sector include both large- and small- landholders.

4.2. Barriers to Scaling up Sustainable Cattle Ranching

Cattle production in Brazil is set to grow; the Brazilian government recently set ambitious targets
for increasing beef and dairy production by 40% [75]. The sustainable growth of the industry is not,
however, guaranteed. To ensure that the cattle industry develops sustainably, improving farmer
livelihoods while protecting the environment, will require a mix of the right financial incentives, efforts
to support training of rural workers and agricultural extension services, and improved monitoring of
cattle supply chains.
Most cattle ranchers adopt good agricultural practices because of the expected improvements in
productivity and profitability [76]. However, implementation costs and difficulty in accessing credit
are barriers for many producers. Among producers surveyed in Mato Grosso regarding adoption
of good agricultural practices, 18% cited financial constraints as a barrier to adoption [76], and high
implementation costs are also an important barrier for four of the six cattle initiatives described in this
article (Figure 12).

Figure 12. (a) The most important barriers to the implementation of sustainable cattle initiatives,
and (b) the solutions to these barriers, as identified in the survey of the organizations running the six
sustainable cattle ranching initiatives described in this article.

83
Sustainability 2018, 10, 1301

Sustainable growth in the cattle industry must also combine productivity improvements with the
protection of native vegetation. In the Amazon biome, farmers are required to keep 80% of their land
under forest (the threshold is set at 50% for small properties and properties in Ecological and Economic
Zoning areas), and must reforest any land deforested above this threshold, or purchase certificates
through the nascent forest trading scheme to compensate [77]. As the forest certificate market is not
yet operating at scale, farmers currently rely on on-site reforestation for legal compliance, and the costs
can be substantial. The do Campo à Mesa and Novo Campo Program initiatives report reforestation
costs of R$868–6068/ha and R$2360–9654/ha, respectively. These figures are roughly equivalent to the
costs of pasture intensification and implementation of GAP. Unfortunately, even where farmers can
access credit, no credit lines currently support costs of compliance with the Forest Code [37].
The financial barriers to improved cattle production and compliance with the Forest Code can,
however, be overcome by developing the right private and public incentives for producers (Figure 12).
Currently, farmers receive the same price for their product, regardless of their environmental
management. This could be fixed by the development of sustainable beef price premiums and
certification schemes, such as the “Standard for Sustainable Cattle Production Systems” developed by
the Sustainable Agricultural Network, which delivers a financial reward to producers implementing
good practices [78]. Similarly, agricultural credit can be leveraged for sustainability, by making access
to agricultural credit contingent on the adoption of sustainable ranching practices, and by supporting
the costs of meeting the requirements of the Forest Code.
As an example of sustainable credit, in 2010 Brazil created the landmark ABC Program, one of
the world’s first credit lines for low carbon agriculture [79], which supports the costs of restoring
degraded pasture and the implementation of integrated crop-livestock-forestry systems. The impact of
the ABC Program has, however, been hampered by bureaucratic issues, unfavorable interest rates, and
a lack of public awareness. Producers perceive the ABC program as being complex, slow, and overly
bureaucratic [76]—posing a particular problem for small producers [80]. The ABC Program is often
out-competed by other credit lines; its interest rates (7.5–8% per year) are double that of loans available
through the National Rural Credit System, Brazil’s main source of agricultural credit [79]. Public
awareness is also a problem. Surveys in the Alta Floresta region of Mato Grosso show that most
producers have not heard of the ABC Program and are not familiar with the concept of sustainable
credit lines [80]. Only 10% of the ABC Program’s budget is spent in the northern states, which make
up the majority of the Amazon biome [81]. Overall, sustainable credit lines make up only 1.9% of
all agricultural credit in Brazil [79], and there are currently no sustainable credit lines which are
specifically aimed at smallholders, though these could be created within the existing National Program
for Strengthening Family Agriculture (Portuguese acronym, PRONAF) [79].
The widespread adoption of sustainable cattle ranching will, of course, require more than just
the correct mix of financial incentives. Barriers are also posed by a shortage of trained labor, farmer
risk aversion, and the complexity of cattle supply chains. Improved farm performance cannot be
achieved without the adequate training of farm staff. The lack of qualified labor is, however, acute
in both beef and dairy production [76,82]. Sixty-five percent of ranchers surveyed in Alta Floresta,
Mato Grosso, cited a shortage of qualified labor as the main barrier to the adoption of good agricultural
practices [76]. Access to agricultural extension services is also limited [11]. Four-fifths of dairy farmers
in Mato Grosso, for example, have never received technical assistance [28].
Farmer psychology also plays an important role (Figure 12). High-yielding cattle ranching
costs more in the short term, though it generates positive returns in the longer-term (Tables 2 and 3).
Many cattle ranchers are, however, risk averse [4] or not motivated by profit-maximization [83], and the
transition from low-input, low-risk extensive systems to intensive pasture management requires to
some degree a shift in mindset. Improved farm management begins with improved record-keeping,
which is a foreign concept to most producers [4]. Rotational grazing systems also require that cattle are
moved more frequently. Nelore cattle breeds have a reputation as being difficult to handle, though this
is in large part because in extensive systems they are not used to contact with farm staff. While regular

84
Sustainability 2018, 10, 1301

contact with farm laborers does improve their temperament [84], farmers can at first take some
convincing about the feasibility of new management practices. The required shift in mindset is perhaps
even greater for the adoption of silvopastoral systems and mixed grass-legume pastures. Farmers
used to thinking of cattle as animals which graze grass may be initially reluctant to incorporate trees
or herbaceous legumes (usually considered as undesirable species) into pasture as a source of forage
and fertilizer.
These psychological barriers can perhaps be overcome by increasing familiarity with high-yielding
systems, which remains low [80]. Awareness can be raised by establishing demonstration units on real
farms, as in the six initiatives described in this article, and open-farm field days so that local farmers
can witness and learn about new management options (Figure 11). As Brazilian farmers’ receive most
of their farming advice from other farmers [85], word-of-mouth dissemination of new technologies
is critical, and can be effective, as seen in the experiences of legume pastures in Acre. The existence
of local champions, long-term commitment of key players, and strategic partnerships among local
stakeholders are also key to successful wide adoption of intensive cattle production systems [41].
Finally, there are structural barriers to sustainable cattle ranching. Cattle supply chains are
complex, which means that deforestation is difficult to eradicate. While market initiatives (such as
the “Terms of Adjustment of Conduct” and “G4” agreements) require meatpacking companies to
block sales from properties with illegal deforestation (the G4 prohibits new deforestation altogether),
this applies only to properties which supply cattle directly to slaughterhouses. As cattle may be born
on one ranch, reared on a second, and fattened on a third, leakage is widespread. Though these
agreements have reduced deforestation among the direct suppliers of slaughterhouses, it has not
led to overall reductions in deforestation [71]. To permit growth of the Brazilian beef industry while
reducing deforestation will therefore require efforts to reduce leakage. This could be achieved either by
monitoring the movements of individual cattle, for example, using unique ear tags, or by monitoring
farm-to-farm movement of batches of cattle. This information is already collected as part of the Guide
to Animal Transport (GTA) used to track animal sanitation and health, but it is not used for monitoring
environmental compliance.
While the barriers to scaling-up high-yielding cattle ranching in the Amazon are numerous, there
is cause for optimism. First, cattle productivity is already increasing in most regions of Brazil [13,86].
Second, the example of leguminous pasture adoption in Acre shows that local demonstration farms
can lead to technology diffusion at a regional scale in the Amazon. Third, though focused in southern
Brazil, lessons can be learned from the dairy extension initiative, the Projeto Balde Cheio (“Full Bucket”
project in English). The program began in 1999 in two municipalities in the states of São Paulo
and Minas Gerais, where demonstration units were established on twelve farms. Operating on a
budget of only R$5000–45,000 (US$5000–23,000) per year, agricultural extension officers from Embrapa
worked with farmers to introduce a package of new practices, including improved farm book-keeping,
soil conservation, pasture fertilization, and rotational management. On average, family farmers
who joined the program increased milk production three-fold [82], with higher productivity arising
from a combination of more lactating cows/area (31%), higher productivity/cow (24%), and better
labor performance (37%), while using less land area (−7%). The initiative has since expanded, as the
number of farmers assisted rose from 400 in 2010 to more than 3000 in 2012, and is now present in
483 municipalities nationwide, including farms in Rondônia, Pará and Amazonas, within the Amazon
biome (Table S4, Supplementary Material).

5. Conclusions
As cattle ranching makes up the majority of agricultural land and productivity is still well below
its sustainable potential, improvements in cattle productivity are key to the sustainable intensification
of Brazilian agriculture. We present results from six cattle ranching initiatives which have achieved
higher productivity and profitability in the Brazilian Amazon, while also supporting compliance with
the Forest Code. These initiatives are, for the most part, still young and so we conclude by setting out

85
Sustainability 2018, 10, 1301

three key conditions which are required to mainstream sustainable cattle ranching in the Amazon.
If these conditions are met, we believe that the Brazilian beef industry can profitably produce more on
less land and thereby facilitate growth in the agricultural sector while protecting Brazil’s remaining
native vegetation.

(1) Large-scale knowledge transfer—long-term funding and support is required for farmer-centered
agricultural extension services, which increase awareness of high-yielding technologies and
support small- and large-holders alike to adopt appropriate farming practices.
(2) Financial support for sustainable cattle ranching—farmers must be incentivized to adopt
sustainable ranching practices, both through competitive, sustainable credit lines and through
market signals. Rural credit lines should include sustainability criteria, and should help farmers
not only increase agricultural production, but also meet the costs of Forest Code compliance.
Market signals also matter, and just as some slaughterhouses offer price-premiums for high meat
quality, price-premiums for GAP would encourage farmer uptake.
(3) Increase transparency in cattle supply chains—efforts by some slaughterhouses to monitor direct
suppliers are a step in the right direction, but do not go far enough. All slaughterhouses should
monitor both indirect and direct cattle suppliers, and monitoring efforts should be independently
audited and publicly reported, so that deforestation may ultimately be eliminated from cattle
supply chains.

Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/4/1301/s1,

supplementary text about the risks of cattle intensification; Tables S1–S4, and Figures S1 and S2.
Acknowledgments: We thank Fabio Ramos, Daniel Silva, André Novo, Artur Camago, Abdias Machado,
Kemel Kalif, Márcio Rangel, Ezequiel Rodrigues do Valle, Marcelo Stabile, Mariano Cenamo, João Pedro Pio,
Toby Gardner, Ben Phalan, Javier Godar, Livia Matyucheva, Priscila da Cunha Lessa, and Jose Guerrero for their
input at various stages of the project. Erasmus K.H.J. zu Ermgassen was funded by BBSRC grant BB/J014540/1
and the Tim Whitmore Trust Fund. Funding for open access publishing come from BBSRC grant BB/J014540/1.
Author Contributions: Erasmus K.H.J. zu Ermgassen co-designed the study, wrote the survey, collected the data,
analysed the data, and led on the writing of the manuscript. Bernardo B.N. Strassburg and Agnieszka Latawiec
co-designed the study; Melquesedek Pereira de Alcântara, Francisco Beduschi Neto, Murilo M. F. Bettarello,
Genivaldo de Brito, Gabriel C. Carrero, Eduardo de A.S. Florence, Edenise Garcia, Eduardo Trevisan Gonçalves,
Casio Trajano da Luz, Giovanni M. Mallman, and Judson F. Valentim provided data, and all co-authors contributed
substantially to the writing of the manuscript.
Conflicts of Interest: This manuscript reports the results of six initiatives which have increased the productivity of
cattle ranching in the Brazilian Amazon. Many of the authors (Melquesedek Pereira de Alcântara, Francisco Beduschi
Neto, Murilo M.F. Bettarello., Genivaldo de Brito, Gabriel C. Carrero, Eduardo de A.S. Florence, Edenise Garcia,
Eduardo Trevisan Gonçalves, Casio Trajano da Luz, Giovanni M. Mallman, Bernardo B.N. Strassburg, Judson F.
Valentim, and Agnieszka Latawiec) were directly involved in the development of these initiatives. The founding
sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of
the manuscript, and in the decision to publish the results.

References
1. FIESP Outlook FIESP 2026: Projections for Brazilian Agribusiness; Federação das Indústrias do Estado de São
Paulo: São Paulo, Brazil, 2016.
2. Brazil Intended Nationally Determined Contribution towards Achieving the Objective of the United Nations
Framework Convention on Climate Change. Available online: http://www4.unfccc.int/submissions/
INDC/Published%20Documents/Brazil/1/BRAZIL%20iNDC%20english%20FINAL.pdf (accessed on
16 April 2018).
3. Strassburg, B.B.N.; Latawiec, A.E.; Barioni, L.G.; Nobre, C.A.; da Silva, V.P.; Valentim, J.F.; Vianna, M.;
Assad, E.D. When enough should be enough: Improving the use of current agricultural lands could meet
production demands and spare natural habitats in Brazil. Glob. Environ. Chang. 2014, 28, 84–97. [CrossRef]
4. Barbosa, F.A.; Soares Filho, B.S.; Merry, F.D.; de Oliveira Azevedo, H.; Costa, W.L.S.; Coe, M.T.; da Silveira
Batista, E.; Maciel, T.C.; Sheepers, L.C.; de Oliveira, A.R.; et al. Cenários para a Pecuária de corte Amazônica;
Universidade Federal de Minas Gerais: Belo Horizonte, Brazil, 2015; p. 154.

86
Sustainability 2018, 10, 1301

5. De Oliveira Silva, R.; Barioni, L.G.; Queiroz Pellegrino, G.; Moran, D. The role of agricultural intensification
in Brazil’s Nationally Determined Contribution on emissions mitigation. Agric. Syst. 2018, 161, 102–112.
[CrossRef]
6. Cohn, A.S.; Mosnier, A.; Havlik, P.; Valin, H.; Herrero, M.; Schmid, E.; O’Hare, M.; Obersteiner, M.
Cattle ranching intensification in Brazil can reduce global greenhouse gas emissions by sparing land from
deforestation. Proc. Natl. Acad. Sci. USA 2014. [CrossRef] [PubMed]
7. De Oliveira Silva, R.; Barioni, L.G.; Hall, J.A.J.; Moretti, A.C.; Fonseca Veloso, R.; Alexander, P.; Crespolini, M.;
Moran, D. Sustainable intensification of Brazilian livestock production through optimized pasture restoration.
Agric. Syst. 2017, 153, 201–211. [CrossRef]
8. Bogaerts, M.; Cirhigiri, L.; Robinson, I.; Rodkin, M.; Hajjar, R.; Costa Junior, C.; Newton, P. Climate change
mitigation through intensified pasture management: Estimating greenhouse gas emissions on cattle farms in
the Brazilian Amazon. J. Clean. Prod. 2017, 162, 1539–1550. [CrossRef]
9. Piccoli, M.L.; Braccini Neto, J.; Brito, F.V.; Campos, L.T.; Bértoli, C.D.; Campos, G.S.; Cobuci, J.A.;
McManus, C.M.; Barcellos, J.O.J.; Gama, L.T. Origins and genetic diversity of British cattle breeds in Brazil
assessed by pedigree analyses. J. Anim. Sci. 2014, 92, 1920–1930. [CrossRef] [PubMed]
10. Townsend, C.R.; de Lucena Costa, N.; de Araújo Pereira, R.G. Aspectos Econômicos da Recuperação de Pastagens
no Bioma Amazônia; EMBRAPA: Porto Velho, Brazil, 2009; p. 28.
11. Valentim, J.F. Desafios e estratégias para recuperação de pastagens degradadas e intensificação da pecuária
a pasto na Amazônia Legal. In Simpósio de Pecuária Integrada; Pereira, D.H., Carneiro e Pedreira, B., Eds.;
Recuperação de Pastagens: Anais; Fundação Uniselva: Cuiabá, Brazil, 2016; pp. 11–56.
12. Dias-Filho, M.B.; Andrade, C.M.S. De Pastagens no Trópico Úmido; Embrapa Amazônia Oriental: Belém, Brazil,
2006; p. 33.
13. Dias, L.C.P.; Pimenta, F.M.; Santos, A.B.; Costa, M.H.; Ladle, R.J. Patterns of land use, extensification, and
intensification of Brazilian agriculture. Glob. Chang. Biol. 2016, 22, 2887–2903. [CrossRef] [PubMed]
14. Bowman, M.S.; Soares-Filho, B.S.; Merry, F.D.; Nepstad, D.C.; Rodrigues, H.; Almeida, O.T. Persistence
of cattle ranching in the Brazilian Amazon: A spatial analysis of the rationale for beef production.
Land Use Policy 2012, 29, 558–568. [CrossRef]
15. Ministério da Agricultura, Pecuária e Abastecimento; Ministério da Ciência, Tecnologia, Inovações e
Comunicações; Ministério do Meio Ambiente. Projeto Terraclass 2012; Embrapa & INPE: Brasília, Brazil, 2014.
16. Börner, J.; Kis-Katos, K.; Hargrave, J.; König, K. Post-Crackdown Effectiveness of Field-Based Forest Law
Enforcement in the Brazilian Amazon. PLoS ONE 2015, 10, e0121544. [CrossRef] [PubMed]
17. Soares-Filho, B.; Moutinho, P.; Nepstad, D.; Anderson, A.; Rodrigues, H.; Garcia, R.; Dietzsch, L.; Merry, F.;
Bowman, M.; Hissa, L.; et al. Role of Brazilian Amazon protected areas in climate change mitigation.
Proc. Natl. Acad. Sci. USA 2010, 107, 10821–10826. [CrossRef] [PubMed]
18. Gibbs, H.K.; Rausch, L.; Munger, J.; Schelly, I.; Morton, D.C.; Noojipady, P.; Soares-Filho, B.; Barreto, P.;
Micol, L.; Walker, N.F. Brazil’s Soy Moratorium. Science 2015, 347, 377–378. [CrossRef] [PubMed]
19. Assunção, J.; Gandour, C.; Rocha, R. Deforestation slowdown in the Brazilian Amazon: Prices or policies?
Environ. Dev. Econ. 2015, 20, 697–722. [CrossRef]
20. Tollefson, J. Deforestation spikes in Brazilian Amazon. Nature 2016, 540. [CrossRef]
21. Carrero, G.; Fearnside, P. Forest Clearing Dynamics and the Expansion of Landholdings in Apuí,
a Deforestation Hotspot on Brazil’s Transamazon Highway. Ecol. Soc. 2011, 16. [CrossRef]
22. Datu Research. Deforestation and the Brazilian beef Value Chain; Datu Research: Durham, NC, USA, 2014.
23. Merry, F.; Soares-Filho, B. Will intensification of beef production deliver conservation outcomes in the
Brazilian Amazon? Elem. Sci. Anth. 2017, 5, 24. [CrossRef]
24. Richards, P.D.; Walker, R.T.; Arima, E.Y. Spatially complex land change: The Indirect effect of Brazil’s
agricultural sector on land use in Amazonia. Glob. Environ. Chang. 2014, 29, 1–9. [CrossRef] [PubMed]
25. IBGE Pesquisa Pecuária Municipal (PPM). Available online: https://sidra.ibge.gov.br/pesquisa/ppm/
quadros/brasil/2015 (accessed on 24 April 2017).
26. PRODES Desflorestamento nos Municipios. Available online: http://www.dpi.inpe.br/prodesdigital/
prodesmunicipal.php (accessed on 26 April 2017).
27. Pacheco, P. Actor and Frontier Types in the Brazilian Amazon: Assessing Interactions and Outcomes
Associated with Frontier Expansion. Geoforum 2012, 43, 864–874. [CrossRef]

87
Sustainability 2018, 10, 1301

28. Gomes, S.T.; Instituto Mato-Grossense de Economia Agropecuária. Diagnóstico da Cadeia do Leite no Estado de
Mato Grosso; Famato, Senar-MT, & Sescoop-MT: Cuiabá, Brazil, 2012; p. 103.
29. Zoccal, R.; Alves, E.R.; Gasques, J.G. Diagnóstico da Pecuária de Leite nacional: Estudo Preliminar. Contribuição
para o Plano Pecuário 2012; Embrapa Gado de Leite: Juiz de Fora, Brazil, 2011.
30. Santana, M.L.; Pereira, R.J.; Bignardi, A.B.; El Faro, L.; Tonhati, H.; Albuquerque, L.G. History, structure, and
genetic diversity of Brazilian Gir cattle. Livest. Sci. 2014, 163, 26–33. [CrossRef]
31. Eurostat Database Agriculture Statistics. Available online: http://ec.europa.eu/eurostat (accessed on 9
January 2014).
32. Livestock Improvement Corporation (LIC); DairyNZ. New Zealand Dairy Statistics 2013–14; Livestock
Improvement Corporation Limited and DairyNZ Limited: Hamilton, New Zealand, 2014; p. 55.
33. IBGE Censo Agropecuário. Available online: http://www2.sidra.ibge.gov.br/bda/acervo/acervo2.asp?e=
v&p=CA&z=t&o=24 (accessed on 21 April 2017).
34. Andrade, C.M.S.; de Santos, D.M.; dos Ferreira, A.S.; Valentim, J.F. Técnicas de Plantio Mecanizado de Forrageiras
Estoloníferas por Mudas; EMBRAPA: Rio Branco, Brazil, 2016; p. 22.
35. Carrero, G.C. Sistemas Silvipastoris com Pastejo Rotacional: Alternativas Sustentáveis para a Produção
Pecuária na Amazônia. In Gestão e Governança Local para a Amazônia Sustentável; notas técnicas; PQGA/IBAM:
Belém, Brasil, 2016; pp. 79–91.
36. Carrero, G.C.; Bettarello, M.; Alcântra, A.; Cenamo, M.C. Sistema extensivo versus sistema silvipastoril
intensivo para pecuária de leite na Amazônia Brasileira: Produtividade, benefícios socioeconômicos e
ecossistêmicos para mitigação e adaptação às mudanças climáticas. In 3◦ Congreso Nacional de Sistemas
Silvopastoriles—VIII Congreso Internacional de Sistemas Agroforestales; Peri, L., Ed.; Ediciones INTA: Santa Cruz,
CA, USA, 2015; pp. 304–308.
37. Garcia, E.; Ramos Filho, F.S.V.; Mallmann, G.M.; Fonseca, F. Costs, Benefits and Challenges of Sustainable
Livestock Intensification in a Major Deforestation Frontier in the Brazilian Amazon. Sustainability 2017,
9, 158. [CrossRef]
38. Marcuzzo, S.F.; de Lima, A. A Programa Novo Campo: Estratégia de Pecuária Sustentável na Amazônia; Instituto
Centro de Vida: Alta Floresta, MT, Brazil, 2015.
39. Sá, C.P.d; Bayma, M.M.A.; Carvalho, B.P. Avaliação dos Impactos da Tecnologia—Recomendação do Amendoim
Forrageiro (Arachis Pintoi) em Pastagens no Acre; EMBRAPA: Rio Branco, Brazil, 2016; p. 18.
40. Valentim, J.F.; Andrade, C.M.S. Tropical kudzu (Pueraria phaseoloides): Successful adoption in sustainable
cattle production systems in the western Brazilian Amazon. In Proceedings of the XX International Grassland
Congress: Offered Papers; Wageningen Academic Publishers: Wageningen, The Netherlands, 2005.
41. Valentim, J.F.; Andrade, C.M.S. Forage peanut (Arachis pintoi): A high yielding and high quality tropical legume
for sustainable cattle production systems in the western Brazilian Amazon. In Proceedings of the XX International
Grassland Congress: Offered Papers; Wageningen Academic Pub: Wageningen, The Netherlands, 2005.
42. Andrade, C.M.S. Produção de ruminantes em pastos consorciados. In Proceedings of the Simpósio SOBRE
MAnejo Estratégico da Pastagem, Viçosa, MG, Brazil, 11–13 November 2010; pp. 171–214.
43. Panerai, A. Amendoim Forrageiro 2008. Available online: https://pt.slideshare.net/AlexandrePanerai/
amendoim-forrageiro-embrapa (accessed on 8 May 2017).
44. De Sá, C.P.; Andrade, C.M.S.; Valentim, J.F. Análise Econômica para a Pecuária de Corte em Pastagens Melhoradas
no Acre; EMBRAPA: Rio Branco, Brazil, 2010; p. 5.
45. Andrade, C.M.S. Importância das Leguminosas Forrageiras para a Sustentabilidade dos Sistemas de
Produção de ruminantes. Available online: http://www.sbprc.famev.ufu.br/sites/sbprc.famev.ufu.br/
files/Carlos%20Maur%C3%ADcio%20Andrade_As%20leguminosas%20e%20a%20sustentabilidade.pdf
(accessed on 20 July 2017).
46. INPE Dados TerraClass 2014. Available online: http://www.inpe.br/cra/projetos_pesquisas/terraclass2014.
php (accessed on 22 May 2017).
47. Valentim, J.F.; Andrade, C.M.S. Perspectives of grass-legume pastures for sustainable animal production in
the tropics. Reunião Annu. Soc. Bras. Zootec. 2004, 40, 142–154.
48. Henderson, B.B.; Gerber, P.J.; Hilinski, T.E.; Falcucci, A.; Ojima, D.S.; Salvatore, M.; Conant, R.T. Greenhouse
gas mitigation potential of the world’s grazing lands: Modeling soil carbon and nitrogen fluxes of mitigation
practices. Agric. Ecosyst. Environ. 2015, 207, 91–100. [CrossRef]

88
Sustainability 2018, 10, 1301

49. Costa, F.S.; Sales, M.F.L.; Freitas, A.C.R.; Souza, C.P. Modeling nitrous oxide emissions in grass and
grass-legume pastures in the western Brazilian Amazon. In International Symposium on Greenhouse Gases in
Agriculture; Embrapa: Brasília, DF, Brazil, 2016; Volume 2.
50. Do Valle, E.R. Lista de verificação: Rebanhos Comerciais; EMBRAPA: Brasília, DF, Brazil, 2013.
51. Cerri, C.C.; Moreira, C.S.; Alves, P.A.; Raucci, G.S.; Castigioni, B.d.A.; Mello, F.F.C.; Cerri, D.G.P.; Cerri, C.E.P.
Assessing the carbon footprint of beef cattle in Brazil: A case study with 22 farms in the State of Mato Grosso.
J. Clean. Prod. 2016, 112, 2593–2600. [CrossRef]
52. Siqueira, T.T.S.; Duru, M. Economics and environmental performance issues of a typical Amazonian beef
farm: A case study. J. Clean. Prod. 2016, 112, 2485–2494. [CrossRef]
53. Piatto, M.; Costa Junior, C. Good Livestock Practices Reduce GHG Emissions and Increase Meat Production in the
Amazon; Imaflora: Piracicaba, SP, Brazil, 2016.
54. International Institute for Sustainabilit (IIS). Análise Econômica de Uma Pecuária Mais Sustentável; International
Institute for Sustainability: Rio de Janeiro, Brasil, 2015; p. 66.
55. PECSA Pecsa—Pecuária Sustentável da Amazônia. Available online: https://pecsa.com.br/pt/ (accessed on
21 July 2017).
56. Cardona, C.A.C.; Naranjo Ramírez, J.F.; Tarazona Morales, A.M.; Murgueitio Restrepo, E.; Chará Orozco, J.D.;
Ku Vera, J.; Solorio Sánchez, F.J.; Flores Estrada, M.X.; Solorio Sánchez, B.; Barahona Rosales, R. Contribution
of intensive silvopastoral systems to animal performance and to adaptation and mitigation of climate change.
Rev. Colomb. Cienc. Pecu. 2014, 27, 76–94.
57. Broom, D.M.; Galindo, F.A.; Murgueitio, E. Sustainable, efficient livestock production with high biodiversity
and good welfare for animals. Proc. R. Soc. B Biol. Sci. 2013, 280. [CrossRef] [PubMed]
58. Burlamaqui Bendahan, A. Système intégré culture-Elevage–Arbre (SILPF) dans l’État du Roraima, Amazonie
Brésilienne. 2015. Available online: http://agritrop.cirad.fr/583402/ (accessed on 19 April 2017).
59. Dalzell, S.; Meat & Livestock Australia. Leucaena: A Guide to Establishment and Management; Meat and
Livestock Australia: Sydney, Australia, 2006; ISBN 978-1-74191-013-1.
60. Marton, S.M.R.R.; Zimmermann, A.; Kreuzer, M.; Gaillard, G. Comparing the environmental performance of
mixed and specialised dairy farms: The role of the system level analysed. J. Clean. Prod. 2016, 124, 73–83. [CrossRef]
61. Carrero, G.C.; Jacauna, M.A.; Sardinha, A.M.; Bettarello, M. Estabelecimento de árvores nativas de interesse
ecológico e econômico para Sistemas Silvipastoris Intensivos em Apuí, Amazônia Brasileira. In III Congresso
Internacional de Sistemas Agroforestales—III Congresso Nacional de Sistemas Silvipastoriles, 2015, Iguazú, Argentina.
3o Congresso de Sistemas Silvipastoriles: VIII Congreso Internacional de Sistemas Agroforestales; Ediciones INTA:
Santa Cruz, CA, USA, 2015; Volume 1, pp. 21–25.
62. Alvim, M.J.; Paciullo, D.S.C.; de Carvalho, M.M.; Aroeira, L.J.M.; Carvalho, L.d.A.; Novaes, L.P.; Gomes, A.T.;
de Miranda, J.E.C.; Ribeiro, A.C.C.L. Sistema de Produção de Leite com Recria de Novilhas em Sistemas Silvipastoris.
EMBRAPA Gado de Leite. Available online: https://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/
Leite/LeiteRecriadeNovilhas/index.htm (accessed on 18 April 2017).
63. Silveira, S.R. Valor Nutritivo de Panicum Maximum, Cultivares Tanzania y Massai, de Acuerdo a Niveles de Sombra
y de Fertilizacio’n Nitrogenada; INTA: Santiago del Estero, Argentina, 2012; pp. 289–293.
64. Crestani, S.; Mendonça, H.; Ribeiro, F.N.; Frederico, M.M.; Almeida, E.X.d; Portela, F.A. Steers performance
in dwarf elephant grass pastures alone or mixed with Arachis pintoi. Trop. Anim. Health Prod. 2013,
45, 1369–1374. [CrossRef] [PubMed]
65. De Goes, R.H.d.T.e.B.; Mancio, A.B.; de Paula Lana, R.; Alves, D.D.; Leão, M.I.; Silva, A.T.S. Recria de
novilhos mestiços em pastagens de Brachiaria brizantha, com diferentes níveis de suplementação, na região
Amazônica. Desempenho animal. Rev. Bras. Zootec. 2005, 34, 1740–1750. [CrossRef]
66. Hoffmann, A.; Moraes, E.H.B.K.; Mousquer, C.J.; Simioni, T.A.; Gomes, F.J.; Ferreira, V.B.; Silva, H.M. Produção de
Bovinos de Corte no Sistema de Pasto-Suplemento no Período Seco. Nativa 2014, 2, 119–130. [CrossRef]
67. Lesama, M.F.; Moojen, E.L. Produção animal em gramíneas de estação fria com fertilização nitrogenada ou
associadas com leguminosa, com ou sem fertilização nitrogenada. Ciênc. Rural 1999, 29, 123–128. [CrossRef]
68. Latawiec, A.E.; Strassburg, B.B.N.; Valentim, J.F.; Ramos, F.; Alves-Pinto, H.N. Intensification of cattle
ranching production systems: Socioeconomic and environmental synergies and risks in Brazil. Animal 2014,
8, 1255–1263. [CrossRef] [PubMed]
69. Angelsen, A. Policies for reduced deforestation and their impact on agricultural production. Proc. Natl. Acad.
Sci. USA 2010, 107, 19639–19644. [CrossRef] [PubMed]

89
Sustainability 2018, 10, 1301

70. Vale, P.M. The Conservation versus Production Trade-Off: Does Livestock Intensification Increase Deforestation?
Evidence from the Brazilian Amazon; Working Paper No. 197. 2014. Available online: http://www.lse.
ac.uk/GranthamInstitute/wp-content/uploads/2014/12/Working-Paper-174-Vale-2014.pdf (accessed on
16 April 2018).
71. Alix-Garcia, J.; Gibbs, H.K. Forest conservation effects of Brazil’s zero deforestation cattle agreements
undermined by leakage. Glob. Environ. Chang. 2017, 47, 201–217. [CrossRef]
72. Phalan, B.; Green, R.E.; Dicks, L.V.; Dotta, G.; Feniuk, C.; Lamb, A.; Strassburg, B.B.N.; Williams, D.R.;
zu Ermgassen, E.K.H.J.; Balmford, A. How can higher-yield farming help to spare nature? Science 2016,
351, 450–451. [CrossRef] [PubMed]
73. Harfuch, L.; Palauro, G.; Zambianco, W.M. Economic Analysis of Investment for the Cattle Ranching Expansion;
INPUT & AGROICONE: São Paulo, Brazil, 2016; p. 8.
74. Valentim, J.F.; da Carneiro, J.C. Quebra da Dormência e Plantio de Puerária em Sistemas de Produção Agropecuários
e Agroflorestais; Embrapa Acre-Sér. Anteriores INFOTECA-E: Rio Branco, Brazil, 1998.
75. Ministério da Agricultura, Pecuária e Abastecimento (MAPA). Plano mais Pecuária; Ministério da Agricultura,
Pecuária e Abastecimento: Brasília, Brazil, 2014.
76. Latawiec, A.E.; Strassburg, B.B.N.; Silva, D.; Alves-Pinto, H.N.; Feltran-Barbieri, R.; Castro, A.; Iribarrem, A.;
Rangel, M.C.; Kalif, K.A.B.; Gardner, T.; et al. Improving land management in Brazil: A perspective from
producers. Agric. Ecosyst. Environ. 2017, 240, 276–286. [CrossRef]
77. Soares-Filho, B.; Rajão, R.; Merry, F.; Rodrigues, H.; Davis, J.; Lima, L.; Macedo, M.; Coe, M.; Carneiro, A.;
Santiago, L. Brazil’s Market for Trading Forest Certificates. PLoS ONE 2016, 11, e0152311. [CrossRef]
[PubMed]
78. Newton, P.; Alves-Pinto, H.N.; Pinto, L.F.G. Certification, Forest Conservation, and Cattle: Theories and
Evidence of Change in Brazil: Cattle certification in Brazil. Conserv. Lett. 2015, 8, 206–213. [CrossRef]
79. Lopes, D.; Lowery, S. Rural Credit in Brazil; 2017. Available online: http://www.forest-trends.org/
documents/files/doc_5016.pdf (accessed on 7 February 2017).
80. Gurgel, A.G.; Costa, C.F.; Barbosa, L.B.C.; Piha, D. Desafios e Restrições dos Produtores Rurais na Adoção de
Tecnologias de Baixo Carbono ABC: Estudo de Caso em Alta Floresta, em Mato Grosso. Fundação Getulio Vargas
(FGV) Centro de Agronegócio (GV Agro), Escola de Economia de São Paulo (EESP), Observatório ABC.
2017. Available online: http://observatorioabc.com.br/wp-content/uploads/2017/05/Sumario_ABC_
AltaFloresta_-1.pdf (accessed on 6 February 2017).
81. Gurgel, A.C.; Costa, C.F.; Belinky, A.; Monzoni, M.; Vendramini, A.; Rocha, F.C.; Martins, S.C. Análise
dos Recursos do Programa ABC; Centro de Estudos em Sustentabilidade da Fundação Getulio Vargas,
Centro de Agronegócio, Escola de Economia de São Paulo, & Aliança pelo Climate Uso da Terra. 2014.
Available online: https://s3-sa-east-1.amazonaws.com/arquivos.gvces.com.br/arquivos_gvces/arquivos/
340/ObsABC_Relatorio2_AnaliseRecursosRegional_Completo.pdf (accessed on 28 April 2015).
82. Novo, A.L.M. Islands of Dairy in a Sea of Sugarcane: The Future of Family Dairy Farming in Brazil; Wageningen
University: Wageningen, The Netherlands, 2012.
83. Garrett, R.; Gardner, T.; Morello, T.; Marchand, S.; Barlow, J.; Ezzine de Blas, D.; Ferreira, J.; Lees, A.; Parry, L.
Explaining the persistence of low income and environmentally degrading land uses in the Brazilian Amazon.
Ecol. Soc. 2017, 22. [CrossRef]
84. Ceballos, M.C.; Góis, K.C.R.; Sant’Anna, A.C.; Paranhos da Costa, M.J.R. Frequent handling of grazing beef
cattle maintained under the rotational stocking method improves temperament over time. Anim. Prod. Sci.
2016. [CrossRef]
85. Pinto, L.F.G.; Hajjar, R.; Newton, P.; Agrawal, A.; Adshead, D.; Bini, D.; Bogaerts, M.; Cirhigiri, L.;
Maguire-Rajpaul, V.A.; González-Chaves, A.; et al. Transitioning to More Sustainable, Low-Emissions Agriculture
in Brazil; GGIAR, CIAT & FutureEarth. 2016. Available online: https://cgspace.cgiar.org/handle/10568/
75631 (accessed on 31 August 2017).
86. Martha, G.B.; Alves, E.; Contini, E. Land-saving approaches and beef production growth in Brazil. Agric. Syst.
2012, 110, 173–177. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

90
 sustainability

Article
Do Large Slaughterhouses Promote Sustainable
Intensification of Cattle Ranching in Amazonia and
the Cerrado?
Ana Beatriz Santos * and Marcos Heil Costa
Department of Agricultural Engineering, Federal University of Viçosa, Viçosa-MG 36570-900, Brazil;
[email protected]
* Correspondence: [email protected]; Tel.: +55-31-3899-1902

Received: 9 August 2018; Accepted: 31 August 2018; Published: 13 September 2018

Abstract: This study investigated the influence of large slaughterhouses on five variables, two related
to environment impact (land use change rate and greenhouse gases emissions (GE)), and three
related to cattle-ranching intensification (protein from crops, calories from crops and stocking rate).
In Amazonia, the results show a reduction of the land use change rate and GE in zones both with and
without the influence of large slaughterhouses. The hypothesis that slaughterhouses are leverage
points to reduce deforestation in the biome was not confirmed. The slaughterhouses also seem
to have no effect on cattle ranching intensification, as protein and calories production increased
significantly in both zones, while the stocking rates did not change in the influence zones. In the
Cerrado, cattle-ranching intensification is a reality, and is occurring independently of the presence
of large slaughterhouses. In conclusion, the results show no evidence that large slaughterhouses
have promoted either cattle-ranching intensification or improvements in the sustainability of the
cattle-ranching activity in Amazonia and the Cerrado.

Keywords: beef supply chain; beef cattle; sustainability assessment; land use change; greenhouse
gases emissions

1. Introduction
In recent decades, the expansion of cattle ranching in Amazonia and the Cerrado has raised
concerns regarding the increase of CO2 emissions associated with beef production. Historically, Brazil’s
largest share of greenhouse gases (GHG) emissions comes from land use change, particularly the
conversion of natural vegetation to pasturelands [1]. Despite the decrease in Brazilian CO2 emissions
between 2005 and 2010 (from 1.7 to 0.3 Mt-CO2 /year), the LULUCF (Land Use, Land Use Change and
Forestry—see Appendix A for a full list of abbreviations) sector emissions still represented 45% of the
total emissions in 2015 [2].
Sustainable intensification of cattle ranching has been proposed as a promising solution to
reconcile the need for increased beef production and the need for reduction of GHG emissions [3,4].
This concept suggests that producing more beef on less land (referred to as intensification) may slow
deforestation and suppression of native Cerrado vegetation and reduce GHG emissions. According
to Strassburg et al. [4], increasing Brazilian pasture productivity to 49–52% of its potential would be
sufficient to meet demands for beef until 2040. In addition, about 14.3 Gt-CO2e could be mitigated; of
this, 87% (12.5 Gt-CO2e ) would be due to the projected reduction in deforestation [4].
In addition to emissions from land use change, cattle ranching is the largest source of methane
(CH4 ) in the country. Together, the LULUCF sector and CH4 emissions from enteric fermentation
represented 58% of Brazilian GHG emissions in 2015 [2]. Several studies have demonstrated that
investments in pasture management and animal feed are able to increase animal production and reduce

Sustainability 2018, 10, 3266; doi:10.3390/su10093266 91 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3266

the time cattle spend in pasture [5–8]. However, grass-feeding is the predominant management system
in the country, and animal-feed supplementation with protein and calories is still uncommon [6].
The low rate of weight gain due to unsupplemented feeding makes the average slaughter age in Brazil
about four years old, twice what it is in the United States [9].
Brazil’s National Policy on Climate Change (PNMC—Política Nacional sobre Mudanças no
Clima) has mandated a reduction of GHG emissions in several economic activities; in agriculture,
it supports the adoption of techniques that make cattle ranching more productive on existing
pasturelands [10]—i.e., intensification. According to Dias et al. [11], the average stocking rate grew
from 0.70 to 1.48 head/ha in the Cerrado and 0.69 to 1.53 head/ha in the Amazon between 1990 and
2010. The adoption of technologies was responsible for a great part of this increase [12], but in various
localities the pasture productivity remains low [11] and there is no evidence that cattle ranching is
increasing in a sustainable way.
In the beef supply chain, slaughterhouses are potential leverage points for promoting sustainable
intensification due to their interactions with ranchers, their location at the agricultural frontier,
and their ability to restrict ranchers’ access to the market [13]. In the last decade, international
campaigns promoted by non-governmental organizations (NGOs) have linked illegal deforestation to
the emergence of large slaughterhouses in Amazonia [14,15]. In July 2009, individual meatpacking
companies in Pará signed the legally binding Terms of Adjustment of Conduct (TAC), which imposes
penalties on companies purchasing from properties with recent illegal deforestation. These agreements
have since been replicated in the states of Acre, Rondônia, Amazonas and Mato Grosso [13]. The four
biggest meatpackers of the country (JBS, Bertín, Marfrig, and Minerva) also signed in 2009 an
agreement with NGO Greenpeace. This agreement imposed that meatpackers would buy only from
Brazilian Amazonia ranches with zero-deforestation and meet standards issued by international
multi-stakeholder commodity roundtables [13,16].
The public concern about the contribution of beef production to forest loss and climate change
demonstrates probable environmental benefits from slaughterhouse market domination as they have a
direct influence on ranchers. Gibbs et al. [13] quantified the responses of four large JBS slaughterhouse
units in southeastern Pará to zero-deforestation agreements signed in 2009. These units respected the
agreement, avoiding trade with ranchers with illegal deforestation on their lands. Besides, there was
a greater adherence to the Rural Environmental Registry (CAR—Cadastro Ambiental Rural) and a
decrease of deforestation on the properties of JBS partners.
Despite the importance of the theme, previous studies have not directly evaluated the
consequences of large slaughterhouses influence on the sustainable intensification of the cattle ranching
activity. Until now, studies have evaluated cattle intensification from an economic point of view [17,18],
as a source of GHG and potential mitigation strategy [3,4,6] and as an outcome of a sample of policies,
certifications or agreements [13,19–21]. To evaluate the sustainable intensification promoted, the
discussion of the role of large slaughterhouses should not be limited to the analysis of deforestation
rates. In this context, it is also necessary to investigate changes in production—mainly the average of
cattle herd per hectare and potential agricultural region—and in relevant environmental variables.
In this study, we evaluated whether large slaughterhouses have been able to promote changes
in their supply areas to meet sustainable intensification. We analyzed five variables: two related to
environmental impact (land use change rate and GHG emissions) and three related to intensification
(protein and calories produced by crops, and stocking rate). For the environmental impact variables,
we investigated whether the slaughterhouses presence promote a decrease of the land use change and
GHG emissions. For the intensification variables, we investigated whether slaughterhouse presence
help to promote improvements in ranching practices as indicated by the increase in calories and protein
produced by crops—nutrients that might ultimately be used for animal supplementation or for other
purposes—and in rangeland stocking rates.

92
Sustainability 2018, 10, 3266

2. Materials and Methods

This work was divided into four parts. First, we selected large slaughterhouses that started
operation approximately midway between 2000 and 2013, and we delimited their influence zones.
Second, we delimited control zones in regions that are far from slaughterhouse influence and outside
both conservation units and indigenous lands. Third, in the influence zones, we tested for changes after
the slaughterhouse started operation, looking specifically at rates of land use change, GHG emissions,
protein from crops, calories from crops, and cattle stocking rates. Finally, we tested for changes in
these variables in the control zones.

2.1. Study Area

The Amazon is the largest biome in Brazil, covering about 49% of the national territory (420 Mha).
In recent decades, cattle ranching has dominated the process of occupation and exploration of this
biome, following government-sponsored colonization projects and incentives [22]. Currently, about
38 million hectares of pasture is located in the Amazon (25% of the national total). Between 1980
and 2013, cattle herds destined for slaughter grew 800% (from 6.24 to 56.59 million head; Figure 1),
which is 58% of the national increase for this period. In addition to the expansion of cattle ranching, a
dramatic increase in the number of slaughterhouses registered at the Federal Inspection Service was
also observed, from 1 in 1980 to 62 in 2016 (Figure 1).

Figure 1. Number of slaughterhouses registered at the Federal Inspection Service and cattle population
in Brazil, Amazonia and the Cerrado over time.

The Cerrado is the second largest biome in Brazil (200 Mha) and the most important region for
cattle ranching, with 56 Mha of pasturelands. The biome contains the largest national herd (66 million
head in 2014), representing 35% of the national total (Figure 1). As part of the new Brazilian agricultural
frontier, the biome is credited as the driver of the country’s ascendance in global agricultural commodity
markets [6]. The number of slaughterhouses registered at the Federal Inspection Service in the Cerrado

93
Sustainability 2018, 10, 3266

biome grew even more dramatically over the last few decades than the number in the Amazon: from 1
in 1980 to 82 in 2016 (Figure 1).

2.2. Period of Study and Datasets

We evaluated the following variables: land use change rate (ΔLU), GHG emissions (GE), protein
from crops (PC), calories from crops (CC), and cattle stocking rate (SR). We obtained ΔLU from the
forest cover dataset produced by Hansen et al. [23], while other agricultural variables were calculated
from the dataset produced by Dias et al. [11]. Due to limitations of forest cover data availability,
the period was 2000–2013.
The SR was obtained by dividing the number of beef cattle by the total pasture area. To construct
the cattle maps, we used data provided by the Municipal Livestock Survey (PPM—Pesquisa Pecuária
Municipal). We estimated the number of cattle destined for beef production by subtracting the number
of dairy cows from the total number of cattle. To convert the tabular PPM data to a gridded cattle
dataset, we calculated the ratio between the number of beef cattle and total pasture area in tabular form
for each municipality in the Amazonian and Cerrado biomes. The total pasture for each municipality
was extracted using Brazilian municipal boundaries polygons (spatial data) provided by IBGE. Due to
the lack of data for certain years of the analysis, we replicated the available data in the missing years.
Then, we constructed yearly maps for number of cattle by multiplying the municipality ratio (tabular
data described above) and the amount of pasture for each grid cell of the municipality (map data).
In the end, each municipality grid cell (i, j) was assigned a number of cattle proportional to that grid
cell’s total pasture area in that year (t).
GE is the sum of GHG emissions due to enteric fermentation and land use change. To estimate
the CO2 emissions due to land use change (E), we prepared a map of live below- and aboveground
biomass (BGB and AGB) for the historic extent of the major vegetation physiognomies of the Amazon
and the Cerrado. Starting from the BGB and AGB values from the LULUCF Reference Report from the
Third National Communication of Brazil to the UNFCCC (United Nations Framework Convention
on Climate Change) [24], we calculated total biomass values and then assigned these values to each
grid cell in the vegetation map prepared by IBGE [25]. For non-forest vegetation physiognomies
or anthropized areas (i.e., land areas transformed by human activity), we assigned biomass values
corresponding to the average of subdivisions of the Brazilian classification system according to the
dominant phytophysiognomy indicated on the vegetation map layer. The final biomass map of the
historic vegetation expressed in Mg dry matter/ha is presented in Appendix B (Figure A1). Using
these data, we obtained the total biomass (in Mg) for each grid cell (i, j) for each year t by multiplying
the biomass values per area (B(i,j) , in Mg dry matter/ha) by the amount of forest area (F(i,j,t) , in ha) in
the grid cell for that year. Then, we calculated the CO2 emissions per pixel (E(i,j,t) , in Tg-CO2 /year) by
subtracting the total carbon in biomass of each grid cell (i, j) for each year (t + Δt) from the previous
year’s value (year t), according to Equation (1),

44   
E(i,j,t) = × 0.485 × 10−6 B(i,j) F(i,j, t) − F(i,j,t+Δt) (1)
12
where 44/12 is used to convert g-C to g-CO2 , 0.485 to convert the dry matter biomass to carbon, and
10−6 to convert Mg to Tg.
We estimated CH4 emissions by enteric fermentation (M) based on the Methane Emissions
from Enteric Fermentation and Animal Manure Management Reference Report of the Third National
Communication of Brazil to the UNFCCC [26]. Initially, we separated each grid cell’s annual value
for head of cattle (C(i,j,t) ) into three animal categories: adult males, adult females and young cattle.
Using the Tier 2 approach described in IPCC [27], we identified the proportion of cattle in each of
these three categories for each state by year (Rc,(i,j,t) , in percent, where c denotes animal category) and
the corresponding emission factors by category (fc(i,j,t) , in kg-CH4 head 1/year−1 ). As the emission
factors and proportions are available only through 2010, we applied the 2010 values for the years 2011,

94
Sustainability 2018, 10, 3266

2012 and 2013. The total CH4 emissions of each biome are presented in Appendix B and compared
with other data. CH4 emissions were converted to CO2 equivalents (CO2e ) considering the GWP100
(Global Warming Potential over a 100-year time interval). The annual emissions per pixel due to enteric
fermentation by cattle (M(i,j,t) , in Tg-CO2e ) were then calculated according to Equation (2),

M(i,j,t) = 28 × 10−9 ∑c C(i,j,t) R(c,i,j,t) f(c,i,j,t) (2)

where 28 is the GWP100 factor, and 10−9 is used to convert kg to Tg. Finally, we calculated the GE
(Tg-CO2e /year) emitted in year t as the sum of the M and E maps.
The CC and PC variables estimate the quantity of calories and protein produced in the region.
These nutrients might be used for animal supplementation or for other purposes. We selected the
three main feed crops used in the country for analysis: maize, soybean and sugarcane. To estimate the
production (in metric tons) of each crop per pixel (i, j) in a year (t), we multiplied the crop productivity
(in metric ton/ha) by the crop planted area (in ha) maps of Dias et al. [11]. Next, we multiplied the
three production maps—soy (Pso ), maize (Pma ) and sugarcane (Psu )—by the dry matter fraction (dc ).
The energy content (ec ) and protein content (pc ) were then used to convert dry matter values into
calorie and protein values, respectively. The values of dc , ec , and pc are given in Table 1 and are typical
of Brazilian crops. Finally, the values for the protein (PC) and calorie (CC) maps were calculated
according to Equations (3) and (4), respectively:
 
PC(i,j,t) = 10−3 Pso so so ma ma su su
(i,j,t) dc pc + P(i,j,t) dc pc + P(i,j,t) dc pc
ma su
(3)
 
CC(i,j,t) = 0.239 × 10−6 Pso so so ma ma su su
(i,j,t) dc ec + P(i,j,t) dc ec + P(i,j,t) dc ec
ma su
(4)

Table 1. Values for dry matter fraction, energy content, and protein content of crops.

Dry Matter (dc ) * Energy Content (ec ) * Protein Content (pc ) * (as a
(Fraction) (MJ/kg of Dry Matter) Fraction of Dry Matter)
Maize 0.88 13.6 0.105
Soy 0.90 14.3 0.420
Sugarcane 0.23 9.10 0.0430
* Values obtained from Cardoso et al. [28].

In Equation (3), the conversion factor 10−3 is the result of multiplying 106 (used to convert tons to
g) and 10−9 (used to convert g to Gg). In Equation (4), the factor 0.239 is used to convert joules (J) to
calories (cal). The factor 10−6 is the result of multiplying 103 (used to convert tons to kg), 106 (used to
convert MJ to J) and 10−15 (used to convert cal to Pcal).

2.3. Mapping of Large Slaughterhouses and Definition of Influence Zones

Beef slaughterhouse production data is usually classified information. To identify large
slaughterhouses for the study, we first searched for those registered at the Federal Inspection Service
(SIF—Sistema de Inspeção Federal). Registration is a condition for trading across states and exporting.
Slaughterhouses not registered at SIF can sell only inside the state and thus are assumed to be small.
To georeference the locations of slaughterhouses, we looked for each unit on Google Maps through the
addresses reported to the Department for Inspection of Animal Products (DIPOA—Departamento de
Inspeção de Produtos de Origem Animal) of the Brazilian Ministry of Agriculture, Livestock and Food
Supply (MAPA—Ministério da Agricultura, Pecuária e Abastecimento). Other information, such as the
opening or closing date, was collected from the National Register of Legal Entities (CNPJ—Cadastro
Nacional de Pessoa Jurídica); registration with CNPJ is legally required to start business activities in
Brazil. To restrict the analysis only to large units, we selected only slaughterhouses with slaughter

95
Sustainability 2018, 10, 3266

capacity greater than 40 head/hour (classes MB1, MB2 and MB3, according to MAPA ordinance
number 82 of 27 February 1976).
We found 144 slaughterhouse units with SIF registration in Amazonia and the Cerrado, including
61 that qualify as large units (42% of the total, Figure 2). As our analysis aims to determine the impact
of the large slaughterhouses, ideally, the analyzed units should have been operating for close to half of
the 2000–2013 study period, so that a “former” period can be compared to a “latter” period of similar
duration. Thus, we selected slaughterhouses with a starting year for operations (yos ) between 2004 and
2008. Only 12 slaughterhouses satisfy this condition and could thus be used. The selected units are
presented in Table 2, and their locations are shown in Figure 2.

Figure 2. Locations of selected large slaughterhouses and large slaughterhouses that were not selected.
Solid and dashed lines represent paved and unpaved roads, respectively.

96
Sustainability 2018, 10, 3266

Table 2. Characteristics of selected slaughterhouses.

Year of Operation
SIF Code Class * Latitude (◦ ) Longitude (◦ ) State Biome
Start (yos )
791 MB1 2006 11◦ 43 S 61◦ 39 W Rondônia Amazonia
3348 MB1 2004 11◦ 54 S 55◦ 30 W Mato Grosso Amazonia
3047 MB2 2006 17◦ 36 S 52◦ 36 W Goiás Cerrado
137 MB3 2008 16◦ 06 S 47◦ 49 W Goiás Cerrado
1723 MB3 2004 12◦ 29 S 49◦ 08 W Tocantins Cerrado
1886 MB3 2006 16◦ 33 S 54◦ 40 W Mato Grosso Cerrado
1940 MB3 2007 7◦ 16 S 48◦ 16 W Tocantins Amazonia/Cerrado
2583 MB3 2008 6◦ 48 S 50◦ 31 W Pará Amazonia
2937 MB3 2005 10◦ 37 S 55◦ 41 W Mato Grosso Amazonia
4149 MB3 2004 8◦ 42 S 63◦ 55 W Rondônia Amazonia
4267 MB3 2004 10◦ 54 S 61◦ 53 W Rondônia Amazonia
4333 MB3 2004 12◦ 43 S 60◦ 10 W Rondônia Amazonia
* MB1 are units with slaughter capacity greater than 80 head/hour and storage capacity greater than 20 t/day; MB2
are units with slaughter capacity greater than 80 head/hour that may or may not have storage capacity; and MB3
are units with slaughter capacity between 40 and 80 head/hour that may or may not have storage capacity.

We define the slaughterhouse influence zone as the likely cattle supply area around a
slaughterhouse. We delimited the influence zone of each slaughterhouse unit by determining the
distance that could realistically be traveled by a cattle truck. We assumed a maximum travel time
of 8 h, which is the maximum travel time tolerated by cattle [29]. To select the truck routes, we
used the Brazilian road network for 2010 prepared by the National Logistics and Transportation Plan
(PNLT—Plano Nacional de Logística e Transporte). To account for vehicular speed limits, we assigned
different velocities for each part of the route. In Brazil, the maximum permissible truck speeds are
90 km/h on paved roads and 60 km/h on unpaved roads (Law number 9503/1997 modified by Law
number 13,281/2016).
However, it is not possible to adopt these speeds as the average. The high center of gravity of
loaded trucks, the poor condition of Northern Brazilian roads [30] and the necessity for stops are some
of the factors limiting driving speeds. Thus, we assumed an average speed of 10 km/h for distances
traveled until reaching a paved or unpaved road, 20 km/h for distances traveled on unpaved roads
and 40 km/h on paved roads. We also delimited intermediary zones spanning travel distances of 2 h,
4 h and 6 h to determine whether the influence on surrounding areas varies with distance from the
slaughterhouse unit.

2.4. Definition of Control Zones

In this study, we also delimited control zones to determine whether the responses of the study
variables occurred only in the influence zones. The control zones were chosen from areas outside
the influence of any of the slaughterhouses selected for this study. The control zones could not be in
areas around other slaughterhouses with slaughter capacity up to 40 head/hour that opened before
2000. We also excluded areas with indigenous lands and conservation units to avoid the effects of
conservation measures. The control zones are of the same size as the average size of the 8 h-influence
zones, and, in the absence of a yos , we chose 2006 to separate the former and latter periods.

2.5. Data Analysis

We analyzed the changes in five variables, two related to environmental sustainability (land
use change rate (ΔLU) and GHG emissions (GE)) and three related to cattle ranching intensification
(protein from crops (PC), calories from crops (CC), and stocking rate (SR)). To determine whether the
changes really were associated with the start of slaughterhouse operations, we performed two tests, T1
and T2 (Figure 3).
In the first test (T1), we tested for change inside the slaughterhouse influence zone (denoted by
superscript S). We used a Wilcoxon paired test to compare the former period (denoted by subscript

97
Sustainability 2018, 10, 3266

F) with the latter period (denoted by subscript L), where the former period included the years from
2000 to yos , and the latter period the years from yos to 2013. Each variable was tested against its
own alternative hypothesis (Ha). To be considered a promoter of intensification, the slaughterhouse
would need to demonstrably influence the ranchers to increase their stocking rate and use calorie
and protein supplementation. By the same token, to be considered a promoter of sustainability, the
slaughterhouse would influence ranchers to reduce vegetation suppression and GHG emissions. For
the two variables related to environmental impacts, we tested whether the slaughterhouses’ start of
operation is associated with decreased ΔLU (Ha : ΔLULS < ΔLUFS ) and GE (Ha: GELS < GEFS ).
For the three variables related to intensification, we tested whether the slaughterhouses’ start of
operation is associated with regionally increasing the feed supply’s PC (Ha: PCLS > PCFS ) and CC (Ha:
CCLS > CCFS ) and the stocking rate SR (Ha: SRSL > SRSF ). We tested these hypotheses for all influence
zone sizes (transportation radius up to 2 h, 4 h, 6 h and 8 h). In the absence of a significant response
(p > 0.05) in T1, no significant change could be reported in that variable (null hypothesis: Ho), and we
would therefore conclude that the slaughterhouse operation had no impact on that variable.

Figure 3. Flow diagram illustrating the analysis.

In the case of a significant response in any of the influence zones in T1, we used a second test
(T2) to determine whether this response occurred only in the influence zones in this period (and not
in the control zones). In T2, we performed a Wilcoxon paired test with the same hypotheses in the
control zones (denoted by superscript C). That is, we tested whether there was a decrease in ΔLU
(Ha : ΔLULC < ΔLUFC ) and GE (Ha: GEC L < GEF ) and an increase in the PC (Ha: PCL > PCF ),
C C C

CC (Ha: CCL > CCF ) and SR (Ha: SR L > SR F ) observed within the control zones between these
C C C C

time periods. A significant response (p ≤ 0.05) in T2 means that the change in this variable was also
observed elsewhere in the biome, outside of the influence zones, so it might not be directly related to
the slaughterhouse. An opposite or neutral response (p > 0.05) means that the change observed in T1

98
Sustainability 2018, 10, 3266

occurred only in the slaughterhouse influence zone, and, in these cases, we would conclude that the
slaughterhouse had an impact on the variable.

3. Results

3.1. Influence and Control Zones

Figure 4 shows the 12 influence zones obtained. The average sizes of the influence zones for
travel times up to 2 h, 4 h, 6 h and 8 h are 0.43 Mha, 1.7 Mha, 4.1 Mha and 7.3 Mha, respectively.
As the delimited extents were based on the travel time of a truck, the sizes of the influence zones vary
according to the road network present near each slaughterhouse.
Due to the proximity between the slaughterhouse units, there are overlaps in some influence
zones. However, just two zones (4267 and 791) have more than 50% of the 8 h zone shared by both
(Figure 4). As the overlap starts at the 4 h travel time, we decided to keep the units separated instead of
joining them so that the analysis has the same number of units per size of influence zone. In addition,
the zones under the influence of slaughterhouses identified by SIF codes 1940, 3348 and 4333 extend
over both biomes. However, just the 1940 SIF code unit was considered in both biome analyses, as a
large percentage of its 8 h area is in the Cerrado biome (60% of the 8 h zone). Thus, five slaughterhouses
were evaluated for the Cerrado, and eight for the Amazon.

Figure 4. Locations of selected large slaughterhouses and their influence zones. Solid and dashed lines
represent the paved and unpaved roads, respectively.

When choosing the control zones, first we excluded 340 Mha in both biomes, 70% in conservation
units and indigenous lands and 30% in areas under the influence of selected slaughterhouses and

99
Sustainability 2018, 10, 3266

slaughterhouses with yos before 2000. We chose eight control areas in the Amazon and five control
areas in the Cerrado (Figure 5). The selected zones have an average size of 7.3 Mha, the same as the
average size of the 8 h influence zones.

Figure 5. Locations of the control zones. The black squares indicate the zone limits. Green areas
indicate areas with the potential to be control zones. White areas indicate influence zones of selected
slaughterhouses and slaughterhouses with yos before 2000.

3.2. Statistical Analysis

In the following sections, we show the results for each influence zone and control zone, separated
by variable. Negative differences indicate a decrease in the variable analyzed with time.

3.2.1. Environmental Impact Variable: Land Use Change Rate (ΔLU)

Table 3 shows ΔLUF and ΔLUL results for the influence zones and the control zones. The first test
(T1), a Wilcoxon paired test, determines whether there is a decrease in ΔLU inside the influence zones
after the slaughterhouse start of operation. In Amazonia, there is a decrease in ΔLU in all influence
zone sizes (travel times up to 2 h, 4 h, 6 h and 8 h), with similar values of probability (p = 0.004,
Table 4). These results across the various sizes of the influence zones indicate that the distance from
the slaughterhouse unit does not influence ΔLU. Results from T2 show that the decrease of ΔLU also
occurs inside the control zones (p = 0.008, Table 4). The similar responses in both the slaughterhouse
influence zones and the control zones during the same period indicate that the decrease of ΔLU might
be not related to the slaughterhouse presence.

100
 Table 3. Former and latter period values for land use change rate (ΔLU, in ha/year) for each influence zone and control zone.

2h 4h 6h 8h Control
SIF Code ΔLUSF (ha/year) ΔLUSL (ha/year) ΔLUSF (ha/year) ΔLUSL (ha/year) ΔLUSF (ha/year) ΔLUSL (ha/year) ΔLUSF (ha/year) ΔLUSL (ha/year) Control Code ΔLUC
F (ha/year) ΔLUC
L (ha/year)
791 6557.552 2387.213 28,446.332 8836.650 61,395.094 19,953.500 92,905.984 30,894.844 1 80,372.484 47,051.168
3348 9407.771 1465.027 34,195.277 7676.226 82,200.266 18,956.490 137,136.984 42,684.102 2 81,378.305 53,318.988
3047 946.861 1135.288 5235.697 5093.823 14,266.354 11,852.601 25,618.500 21,087.488 3 15,819.864 16,464.074
137 250.060 735.411 1786.634 3959.375 7293.791 11,791.568 17,400.232 25,362.859 4 59,520.324 46,821.258
1723 1816.823 1779.501 9388.703 8416.078 22,971.779 19,033.506 36,794.273 31,167.559 5 59,506.941 50,930.031
1886 1868.623 1362.502 9610.937 5900.309 20,900.621 12,623.756 35,851.840 22,329.553 6 117,978.461 46,430.785
Sustainability 2018, 10, 3266

1940 1576.978 1439.517 10,806.022 8332.689 26,263.994 18,966.988 55,317.758 35,559.426 7 105,355.867 38,125.027
2583 2439.150 563.163 9376.688 2705.178 23,052.080 7771.413 42,548.234 14,280.646 8 30,946.521 19,714.889
2937 781.155 469.791 5982.479 2420.442 22,798.094 8578.547 56,155.816 18,531.934 9 35,776.426 38,022.645
4149 4107.312 2648.438 18,282.762 11,317.136 39,151.117 24,151.670 79,550.453 41,369.051 10 39,928.773 36,683.539
4267 3596.003 1793.645 24,930.428 8992.448 64,370.426 20,787.986 122,377.789 38,633.922 11 34,875.188 35,362.727
4333 7961.677 3783.414 22,355.818 10,142.759 47,414.707 18,169.438 76,847.141 27,719.873 12 29,021.994 36,196.199
13 22,420.396 32,550.551

101
Sustainability 2018, 10, 3266

Table 4. Results of Wilcoxon paired tests for T1 and T2 for land use change rate (ΔLU). T1 tests whether
the introduction of large slaughterhouses was associated with the reduction of ΔLU in the influence
zones (Ha: ΔLULS < ΔLUFS ). T2 tests whether reduction of ΔLU also occurred in the control zones (Ha:
ΔLULC < ΔLUFC ).

Latter Values–Former Values (ΔLU)

   
T1 Ha : ΔLUSL < ΔLUSF L < ΔLUF
T2 Ha : ΔLUC C

SIF Control Control

2 h (ha/year) 4 h (ha/year) 6 h (ha/year) 8 h (ha/year)
Code Code (ha/year)
791 −4170.339 −19,609.682 −41,441.594 −62,011.140 1 −33,321.316
3348 −7942.744 −26,519.051 −63,243.776 −94,452.882 2 −28,059.317
1940 −137.461 −2473.333 −7297.006 −19,758.332 3 644.210
2583 −1875.987 −6671.510 −15,280.667 −28,267.588 4 −12,699.066
Amazonia
2937 −311.364 −3562.037 −14,219.547 −37,623.882 5 −8576.910
4149 −1458.874 −6965.626 −14,999.447 −38,181.402 6 −71,547.676
4267 −1802.358 −15,937.980 −43,582.440 −83,743.867 7 −67,230.840
4333 −4178.263 −12,213.059 −29,245.269 −49,127.268 8 −11,231.632
Median −1839.173 −9589.343 −22,262.968 −43,654.335 −20,379.192
p 0.004 * 0.004 * 0.004 * 0.004 * 0.008 *
3047 188.427 −141.874 −2413.753 −4531.012 9 2246.219
137 485.351 2172.741 4497.777 7962.627 10 −3245.234
Cerrado 1723 −37.322 −972.625 −3938.273 −5626.714 11 487.539
1886 −506.121 −3710.628 −8276.865 −13,522.287 12 7174.205
1940 −137.461 −2473.333 −7297.006 −19,758.332 13 10,130.155
Median −37.322 −972.625 −3938.273 −5626.714 2246.219
p 0.500 NS 0.156 NS 0.156 NS 0.156 NS 0.906 NS
* Indicates significant at 5% level. NS Indicates not significant at 5% level. SIF code 1940 is used in the analyses of
both biomes.

In the Cerrado, T1 shows no decrease in ΔLU (Table 4). This indicates that the slaughterhouses
had no impact on ΔLU inside the slaughterhouse influence zones. Although a drop in ΔLU is observed
in most of the influence zones, due to the small size of the sample, the response is not significant. By
comparison, the T2 test shows interesting results: most of the control zones show increases in ΔLU.
Of the five control zones, four show increases in ΔLU in the latter part of the study period (p = 0.906,
Table 4).

3.2.2. Environmental Impact Variable: Total Greenhouse Gas Emissions (GE)

Table 5 shows GEF and GEL results for the influence zones and control zones. In the Amazon, T1
results show that there is a significant reduction of GE after the slaughterhouses’ start of operation. As
occurred with tests for ΔLU, all zones show the same level of significance, which demonstrates the
absence of a distance influence (p = 0.004, Table 6). The similar responses between ΔLU and GE were
already expected because of the large contribution of land use emissions to the total emissions. After
finding a significant response in the 8 h influence zone for T1, WE used T2 to compare this result with
the response in control areas outside the slaughterhouse influence zones. As occurred with ΔLU, T2
results confirm that the decrease of GE also occurred in the control zones (p = 0.008, Table 6). The T1
and T2 responses demonstrate that the change is observed both inside and outside of the influence
zones during the same period, so the decrease of GE might be unrelated to the slaughterhouse presence.

102
 Table 5. Former and latter period values for greenhouse gas emissions (GE, in Tg-CO2e /year) for each influence zone and control zone.

2h 4h 6h 8h Control
GESF GESL GESF GESL GESF GESL GESF GESL GEC
F GEC
L
SIF Code Control Code
(Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year)
791 4.8 2.5 19 8.2 38 17 57 24 1 59 36
3348 5.6 0.93 20 4.4 44 11 70 24 2 58 39
3047 0.35 0.35 1.9 1.7 5.1 4.4 10 9.3 3 6.1 7.0
137 0.14 0.19 0.86 1.1 3.2 3.9 7.3 8.8 4 42 34
Sustainability 2018, 10, 3266

1723 0.50 0.55 2.3 2.4 5.9 5.6 10 9.6 5 37 32

1886 0.96 0.84 3.3 2.7 6.0 4.7 9.6 7.6 6 64 28
1940 1.0 0.87 6.1 4.2 14 9.4 28 16 7 69 27
2583 1.9 0.58 7.6 2.9 18 7.8 33 14 8 18 11
2937 0.73 0.53 4.1 2.3 14 6.9 30 13 9 15 16
4149 2.3 1.4 9.5 5.6 22 13 46 24 10 7.7 6.8
4267 3.0 2.0 18 9.1 43 19 78 31 11 9.3 9.4
4333 4.2 2.1 12 5.7 25 11 41 18 12 7.3 8.3
13 3.9 5.4

103
Sustainability 2018, 10, 3266

Table 6. Results of Wilcoxon paired tests for T1 and T2 for greenhouse gas emissions (GE). T1 tests
whether the introduction of large slaughterhouses was associated with the reduction of GE in the
influence zones (Ha: GELS < GEFS ) T2 tests whether reduction of GE also occurred in the control zones
(Ha: GECL < GEF ).
C

Latter Values–Former Values (GE)

 
T1 Ha : GESL < GESF L < GEF )
T2 (Ha: GEC C

2h 4h 6h 8h Control Control
SIF Code
(Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) (Tg-CO2e /year) Code (Tg-CO2e /year)
791 −2.3 −11 −22 −33 1 −23
3348 −4.7 −15 −33 −46 2 −19
1940 −0.13 −1.9 −4.8 −12 3 0.94
2583 −1.3 −4.6 −11 −19 4 −7.8
Amazonia
2937 −0.20 −1.8 −7.1 −17 5 −4.4
4149 −0.90 −3.8 −8.4 −22 6 −36
4267 −0.95 −8.8 −24 −47 7 −42
4333 −2.1 −5.9 −14 −23 8 −7.6
Median −1.1 −5.3 −12 −23 −13.6
p 0.004 * 0.004 * 0.004 * 0.004 * 0.008 *
3047 0.0010 −0.16 −0.69 −1.0 9 0.86
137 0.048 0.28 0.71 1.5 10 −0.92
Cerrado 1723 0.046 0.075 −0.27 −0.70 11 0.14
1886 −0.12 −0.65 −1.2 −2.0 12 1.0
1940 −0.13 −1.9 −4.8 −12 13 1.6
Median 0.0010 −0.16 −0.69 −1.0 0.86
p 0.406 NS 0.219 NS 0.156 NS 0.156 NS 0.969 NS
* Indicates significant at 5% level. NS Indicates not significant at 5% level. SIF code 1940 is used in the analyses of
both biomes.

In the Cerrado, T1 results show a nonsignificant response for the reduction of GE inside the
slaughterhouse influence zones. As occurred in Amazonia, the GE results are very similar to the ΔLU
results. In addition, for transportation distances up to 4 h, emissions due to enteric fermentation
appear to have a greater influence on the total emitted. In comparison to what was observed for ΔLU,
where two units show increases inside the influence zones up to 2 h and one up to 4 h, for GE, three
units (SIF codes 3047, 137 and 1723) show increases in GE inside the zones up to 2 h, and two (SIF
codes 137 and 1723) in the zones up to 4 h. According to the analysis framework, the T2 test is not
necessary in the case of negative responses up to 8 h. As was the case with ΔLU analyses, T2 results
looking at GE show that the increases also occur inside the control zones (p = 0.969, Table 6).

3.2.3. Intensification Variable: Protein from Crops (PC)

Table 7 shows PCF and PCL results for the influence zones and control zones. In Amazonia, T1
results show that there was a change in PC inside the influence zones (p ≤ 0.05, Table 8). In addition,
the decrease of p with the increase of influence zone sizes (up to 2 h, 4 h, 6 h, and 8 h) indicates that
distance from the slaughterhouse unit had a likely influence. As T1 results show significant changes
in PC in the influence zones, we use T2 to determine whether the changes occurred only inside the
influence zones. According to T2 results, the increase of PC also occurred in the control zones (p ≤ 0.05,
Table 8), which implies the absence of slaughterhouse impact on this variable.

104
 Table 7. Former and latter period values for protein from crops (PC, in Gg protein) for each influence zone and control zone.

2h 4h 6h 8h Control
SIF Code PCSF (Gg) PCSL (Gg) PCSF (Gg) PCSL (Gg) PCSF (Gg) PCSL (Gg) PCSF (Gg) PCSL (Gg) Control Code PCC
F (Gg) PCC
L (Gg)
791 8.7 15 21 38 36 67 63 1.2 ×102 1 17 37
3348 42 1.1 × 102 2.6 × 102 5.1 × 102 6.2 × 102 1.1 × 103 1.0 × 103 1.8 × 103 2 6.5 18
3047 89 1.2 × 102 3.7 × 102 4.9 × 102 9.3 × 102 1.2 × 103 1.5 × 103 2.0 × 103 3 0.20 1.0
Sustainability 2018, 10, 3266

137 32 49 1.5 × 102 2.5 × 102 4.2 × 102 7.2 × 102 7.5 × 102 1.3 × 103 4 14 22
1723 3.3 10 13 36 28 77 55 1.4 × 102 5 2.0 3.1
1886 1.0 × 102 1.5 × 102 3.5 × 102 4.8 × 102 7.1 × 102 9.5 × 102 1.1 × 103 1.4 × 103 6 5.6 × 102 1.3 × 103
1940 1.2 2.5 6.4 14 34 70 87 1.7 × 102 7 78 1.3 × 102
2583 0.20 0.19 1.4 1.4 4.0 4.2 8.5 10 8 4.4 4.4
2937 1.2 2.7 10 25 35 95 78 2.2 × 102 9 28 80
4149 0.17 0.21 0.36 0.57 0.68 1.3 1.6 3.0 10 2.8 × 102 5.6 × 102
4267 1.1 1.1 7.3 10 21 35 32 61 11 3.2 × 102 5.3 × 102
4333 16 37 63 1.3 × 102 1.6 × 102 2.8 × 102 3.4 × 102 5.4 × 102 12 3.2 × 102 5.1 × 102
13 1.0 × 102 2.7 × 102

105
Sustainability 2018, 10, 3266

Table 8. Results of Wilcoxon paired tests for T1 and T2 for proteins from crops (PC). T1 tests whether
the introduction of large slaughterhouses was associated with the increase of PC in the influence
zones (Ha: PCLS > PCFS ). T2 tests whether the increase of PC also occurred in the control zones (Ha:
PCLC > PCFC ).

Latter Values–Former Values (PC)

T1 (Ha: PCSL > PCSF ) L > PCF )
T2 (Ha: PCC C

SIF Code 2 h (Gg) 4 h (Gg) 6 h (Gg) 8 h (Gg) Control Code Control (Gg)
791 6.3 17 32 59 1 20
3348 66 2.6 × 102 5.2 × 102 8.3 × 102 2 11
1940 1.3 7.6 36 83 3 0.78
2583 −0.011 −0.050 0.19 1.8 4 7.4
Amazonia
2937 1.5 16 60 1.4 × 102 5 1.1
4149 0.049 0.21 0.57 1.4 6 7.1 × 102
4267 −0.032 2.5 14 30 7 51
4333 21 70 1.3 × 102 1.9 × 102 8 −0.069
Median 1.4 12 34 71 9.3
p 0.020 * 0.008 * 0.004 * 0.004 * 0.008 *
3047 32 1.2 × 102 2.8 × 102 4.9 × 102 9 51
137 17 1.0 × 102 3.0 × 102 5.1 × 102 10 2.9 × 102
Cerrado 1723 7.0 23 49 88 11 2.1 × 102
1886 43 1.4 × 102 2.4 × 102 3.5 × 102 12 1.9 × 102
1940 1.3 7.6 36 83 13 1.7 × 102
Median 17 1.0 × 102 2.4 × 102 3.5 × 102 1.9 × 102
p 0.031 * 0.031 * 0.031 * 0.031 * 0.031 *
* Indicates significant at 5% level. SIF code 1940 is used in the analyses of both biomes.

In the Cerrado, based on T1, all sizes of influence zone show an increase in PC after the
slaughterhouse start of operation at the same level of significance (Table 8). The T2 results indicate a
similar increase of PC occurred inside the control zones (p ≤ 0.05, Table 8). These similar responses
indicate that the large slaughterhouses have no impact on the PC.

3.2.4. Intensification Variable: Calories from Crops (CC)

Table 9 shows CCF and CCL results for the study influence zones and control zones. In Amazonia,
T1 shows that there is an increase in CC in all influence zone sizes (up to 2 h, 4 h, 6 h and 8 h). As
occurred with PC, there is an influence of distance from the slaughterhouse, with p decreasing along
with increase of zone size. T2 shows that the increase in CC between the two time periods also occurs
inside the control zones (p = 0.020, Table 10). The similar responses in T1 and T2 indicate that the
increase of CC might not be related to the slaughterhouse presence.

106
 Table 9. Former and latter period values for calories from crops (CC, in Pcal) for each influence zone and control zone.

2h 4h 6h 8h Control
SIF Code CCSF (Pcal) CCSL (Pcal) CCSF (Pcal) CCSL (Pcal) CCSF (Pcal) CCSL (Pcal) CCSF (Pcal) CCSL (Pcal) Control Code CCC
F (Pcal) CCC
L (Pcal)
791 0.13 0.24 0.33 0.58 0.53 1.0 0.84 1.6 1 0.47 0.77
3348 0.39 1.2 2.4 5.6 5.8 12 10 20 2 0.17 0.32
3047 1.1 1.8 4.4 7.4 11 18 18 30 3 0.0067 0.015
Sustainability 2018, 10, 3266

137 0.45 0.74 2.1 3.6 5.3 9.7 10 17 4 0.29 0.33

1723 0.037 0.10 0.15 0.36 0.34 0.78 0.75 1.7 5 0.057 0.070
1886 1.1 1.7 3.7 5.7 7.3 11 11 17 6 5.4 14
1940 0.016 0.029 0.092 0.17 0.47 0.82 1.1 1.9 7 0.77 1.3
2583 0.0063 0.0058 0.043 0.039 0.11 0.11 0.22 0.22 8 0.070 0.056
2937 0.017 0.031 0.11 0.28 0.37 1.0 0.80 2.4 9 0.80 1.7
4149 0.0052 0.0055 0.011 0.015 0.021 0.030 0.048 0.067 10 3.0 6.1
4267 0.034 0.033 0.18 0.22 0.38 0.58 0.52 0.93 11 3.3 5.6
4333 0.16 0.41 0.62 1.5 1.6 3.2 3.4 6.0 12 3.8 5.8
13 1.1 2.9

107
Sustainability 2018, 10, 3266

Table 10. Results of Wilcoxon paired tests for T1 and T2 for calories from crops (CC). T1 tests whether
the introduction of large slaughterhouses was associated with the increase of CC in the influence
zones (Ha: CCLS > CCFS ).T2 tests whether the increase of CC also occurred in the control zones (Ha:
CCLC > CCFC ).

Latter Values–Former Values (CC)

T1 (Ha: CCSL > CCSF ) L > CCF )
T2 (Ha: CCC C

SIF Code 2 h (Pcal) 4 h (Pcal) 6 h (Pcal) 8 h (Pcal) Control Code Control (Pcal)
791 0.10 0.26 0.45 0.79 1 0.30
3348 0.78 3.2 6.6 11 2 0.14
1940 0.012 0.073 0.35 0.86 3 0.0085
2583 −0.00056 −0.0043 −0.0065 −0.0022 4 0.037
Amazonia
2937 0.014 0.17 0.67 1.6 5 0.013
4149 0.00027 0.0034 0.0090 0.019 6 8.8
4267 −0.0012 0.045 0.20 0.40 7 0.58
4333 0.26 0.86 1.6 2.7 8 −0.014
Median 0.013 0.12 0.40 0.82 0.090
p 0.039 * 0.012 * 0.008 * 0.008 * 0.020 *
3047 0.76 3.0 7.3 13 9 0.90
137 0.28 1.5 4.3 7.9 10 3.1
Cerrado 1723 0.063 0.21 0.43 0.91 11 2.3
1886 0.58 1.9 3.8 5.9 12 2.1
1940 0.012 0.073 0.35 0.86 13 1.8
Median 0.28 1.5 3.8 5.9 2.1
p 0.031 * 0.031 * 0.031 * 0.031 * 0.031 *
* Indicates significant at 5% level. SIF code 1940 is used in the analyses of both biomes.

In the Cerrado, T1 shows that there is an increase in CC (Table 10). All influence zones show a
significant response in T1, which indicates a change occurred after slaughterhouse start of operation.
As the response of the 8 h influence zone is significant, we use T2 results to determine whether the
observed result also occurred inside the control zones. The T2 results do indicate an increase of CC in
the control zones (p ≤ 0.05, Table 10), which means that the increase of CC might be unrelated to the
slaughterhouse presence.

3.2.5. Intensification Variable: Stocking Rate (SR)

Table 11 shows SRF and SRL results for the study influence zones and control zones. In Amazonia,
T1 results indicate that SR is not impacted by the slaughterhouse start of operation, with all sizes of
influence zone showing nonsignificant responses for the change (p > 0.05, Table 12). As T1 is negative,
T2 is not necessary to prove the impact of the slaughterhouse. However, contrary to the results for the
slaughterhouse influence zones, the control zones show a significant increase in the SR between time
periods (p ≤ 0.05, Table 12).

108
 Table 11. Former and latter period values for stocking rate (SR, in head/ha) for each influence zone and control zone.

2h 4h 6h 8h Control
SRSF SRSL SRSF SRSL SRSF SRSL SRSF SRSL Control SRC
F SRC
L
SIF Code
(head/ha) (head/ha) (head/ha) (head/ha) (head/ha) (head/ha) (head/ha) (head/ha) Code (head/ha) (head/ha)
791 2.023 1.915 1.990 1.855 1.946 1.856 1.936 1.873 1 0.981 1.073
3348 0.717 0.753 0.867 0.915 1.066 1.117 1.194 1.240 2 1.204 1.554
Sustainability 2018, 10, 3266

3047 0.875 1.002 0.953 1.055 0.968 1.059 1.033 1.124 3 0.249 0.286
137 1.011 1.257 0.866 1.143 0.821 1.119 0.886 1.184 4 1.452 1.504
1723 0.811 1.060 0.858 1.181 0.845 1.144 0.834 1.115 5 1.342 1.684
1886 1.543 2.033 1.130 1.433 0.980 1.186 0.921 1.073 6 1.458 1.588
1940 0.984 1.043 0.993 1.081 1.025 1.146 1.024 1.150 7 1.589 2.018
2583 2.532 2.672 1.817 1.774 1.628 1.522 1.509 1.423 8 0.584 1.453
2937 2.085 1.850 1.913 1.744 1.782 1.719 1.708 1.728 9 0.968 1.267
4149 1.347 1.668 1.407 1.604 1.421 1.691 1.577 1.902 10 0.656 0.905
4267 1.826 1.925 1.835 1.971 1.866 2.014 1.855 2.036 11 0.653 0.974
4333 1.237 1.075 1.756 1.721 1.869 1.815 1.794 1.821 12 0.612 0.936
13 0.512 0.530

109
Sustainability 2018, 10, 3266

Table 12. Results of Wilcoxon paired test for T1 and T2 for stocking rate (SR). T1 tests whether the
introduction of large slaughterhouses was associated with the increase of SR in the influence zones (Ha:
SRSL > SRSF ). T2 tests whether the increase of SR also occurred in the control zones (Ha: SRCL > SRCF ).

Latter Values–Former Values (SR)

T1 (Ha: SRSL > SRSF ) L > SRF )
T2 (Ha: SRC C

2h 4h 6h 8h Control Control
SIF Code
(Head/ha) (Head/ha) (Head/ha) (Head/ha) Code (Head/ha)
791 −0.108 −0.135 −0.090 −0.063 1 0.092
3348 0.036 0.048 0.051 0.046 2 0.350
1940 0.059 0.088 0.121 0.126 3 0.037
2583 0.140 −0.043 −0.106 −0.086 4 0.052
Amazonia
2937 −0.235 −0.169 −0.063 0.020 5 0.342
4149 0.321 0.197 0.270 0.325 6 0.130
4267 0.099 0.136 0.148 0.181 7 0.429
4333 −0.162 −0.035 −0.054 0.027 8 0.869
Median 0.048 0.007 −0.002 0.037 0.236
p 0.473 NS 0.371 NS 0.320 NS 0.125 NS 0.004 *
3047 0.127 0.102 0.091 0.091 9 0.299
137 0.246 0.277 0.298 0.298 10 0.249
Cerrado 1723 0.249 0.323 0.299 0.281 11 0.321
1886 0.490 0.303 0.206 0.152 12 0.324
1940 0.059 0.088 0.121 0.126 13 0.018
Median 0.246 0.277 0.206 0.152 0.299
p 0.031 * 0.031 * 0.031 * 0.031 * 0.031 *
* Indicates significant at 5% level. NS Indicates not significant at 5% level. SIF code 1940 is used in the analyses of
both biomes.

In the Cerrado, all sizes of influence zone show an increase in SR after the start of operation of
the slaughterhouses studied (p = 0.031, Table 12). According to T2, the control zones have the same
results as the influence zones (p = 0.031, Table 12). These similar responses indicate that the large
slaughterhouses are not directly responsible for SR increases in their influence zones in the Cerrado.

4. Discussion
Regarding the hypothesis that large slaughterhouses promote sustainable agricultural
development and cattle ranching intensification, we expected to find significant reductions in
variables that measured environmental impact (ΔLU and GE) and increases in variables that measured
intensification (PC, CC, and SR) after the start of slaughterhouse operations. In Amazonia, the results
show that there is a significant decrease in ΔLU and GE inside the slaughterhouse influence zones.
However, since the same change happened in the control zones, this decrease might not be caused
directly by the slaughterhouse presence, and might instead be part of the downward trend of
deforestation over the period between 2004 and 2013 [31,32]. For agricultural intensification variables
in Amazonia, PC and CC show a significant increase in both the influence and control zones, while
SR does not show change in the areas under slaughterhouse influence. In the Cerrado, results for all
variables are similar in the control and influence zones. Nonsignificant decreases in ΔLU and GE and
significant increases of PC, CC, and SR are observed in the control zones as well as the influence zones.
The decrease in ΔLU observed both inside and outside the slaughterhouse influence zones in
Amazonia demonstrates not slaughterhouse influence, but the power of conservation programs
and other policies for forest protection [31,33–35]. In addition to the protection granted by the
Brazilian Forest Code and monitoring programs such as the Program for Satellite Monitoring of
the Brazilian Amazon Forest (PRODES—Projeto de Monitoramento da Floresta Amazônica Brasileira
por Satélite) and the System for Detection of Deforestation in Real Time (DETER—System for Detection
of Deforestation in Real Time), the private sector signed ambitious agreements—cattle agreements

110
Sustainability 2018, 10, 3266

in 2009 and a Soy Moratorium in 2006 [36]—to further protect the native vegetation. The effective
contribution of each measure is difficult to disentangle, but the combined result of these actions was a
great success. According to INPE [32] the rate of forest loss in the Brazilian Amazon dropped from
more than 2.7 Mha/year in 2004 to an average of 0.6 Mha/year in 2013, reaching the lowest rates
since 1988.
Unfortunately, the same did not occur in the Cerrado. The decrease of ΔLU did not happen inside
all influence zones. In the control zones, the ΔLU results indicate that there is increased suppression
of Cerrado vegetation in areas away from large slaughterhouse influence. This may be linked with
the absence of an effective vegetation suppression monitoring system in the biome, and the more
permissive New Forest Code, which has allowed more legal suppression since 2012 [35]. Some
studies [36,37] have also warned about a possible leakage of agriculture from Amazonia to the Cerrado
due to the stricter conservation policies in Amazonia. According to the most recent official data
available, 0.725 Mha was suppressed in the Cerrado between 2010 and 2011, which was 12% greater
than observed in the previous period (0.647 Mha, between 2009 and 2010 [38]. In addition, a recent
report released by Mighty Earth and Rainforest Foundation Norway (RFN) claimed that multinational
companies are linked to massive and systematic suppression of native vegetation in areas of Cerrado
in MATOPIBA (an acronym created from the first two letters of the states of Maranhão, Tocantins,
Piauí and Bahia). The report found that areas operated by the investigated companies had 0.697 Mha
of vegetation suppressed from 2011 to 2015 [39].
GE results reflect ΔLU results, as land use emissions dominate GE in both biomes. In Amazonia,
even with the increase of cattle between 2000 and 2013 (from 29 to 56 million head), the emissions from
enteric fermentation are not enough to exceed the emissions from land use; this result was expected
due to the high Amazonian biomass. In the Cerrado, the emissions from enteric fermentation dominate
GE in the influence zones up to 4 h. For GE, by contrast with the results observed for ΔLU, three
slaughterhouse units showed an increase in the areas of influence up to a 2 h driving radius, and two,
in a radius up to 4 h. This response suggests that, in the zones near the slaughterhouses, the native
vegetation has already been suppressed for the most part, making the emissions contributions from
enteric fermentation more prominent than those from land use change.
The PC and CC results show that there has been an increase in the production of protein and
calories in both biomes. In Amazonia, the p calculated for the various influence zone sizes show that
the farther the distance from the slaughterhouse, the greater the increase in both variables. The most
likely reason for this is that areas closer to these slaughterhouses are dominated by pasture, which
is unlikely to be converted to new cropping areas. According to Dias et al. [11], the Amazon and
Cerrado experienced expansion of crop area and increase in production in recent decades, especially
for soybeans. Considering both biomes, soybean production grew from 7.4 million tons in 1990 to
approximately 45.2 million tons in 2010 [11]. As one could expect, our results indicate that the increases
of PC and CC are not related to the slaughterhouses’ presence. However, the large increases in crop
production around slaughterhouses may contribute to future increases in animal feed availability in
the region.
The SR results for Amazonia indicate that these pastures have a stable stocking rate probably
related to stagnant cattle ranching technology. To complement the discussion about SR, we performed
two additional tests. First, we performed a Mann−Whitney test to compare the SR of the control and
influence zones before the year of start of operation. In this test, we aimed to verify whether the large
slaughterhouses we studied were installed in areas with high values of SR. According to the result
(Table 13), before the slaughterhouse start of operation in the Amazon, the SR in the influence zones
was greater than the SR observed in the control zones (p = 0.031, Table 13). This is an indication that
big companies prefer to install slaughterhouse units in areas with high production, to ensure supply to
their large processing capacity.

111
Sustainability 2018, 10, 3266

Table 13. Results of Mann-Whitney test comparing SRSF and SRCF in Amazonia.

Former Period (Ha: SRSF = SRC

F)
SIF Code SRSF (Head/ha) Control Code F (Head/ha)
SRC
791 1.936 1 0.981
3348 1.194 2 1.204
1940 1.024 3 0.249
2583 1.509 4 1.451
2937 1.708 5 1.342
4149 1.577 6 1.458
4267 1.855 7 1.589
4333 1.794 8 0.584
Median 1.643 1.273
p 0.031 *
* Indicates significant at 5% level.

In the second test (Table 14), to verify the stagnation of the SR inside the slaughterhouses influence
zones, we performed a Mann–Whitney test to compare the SR of the control and influence zones after
the start of slaughterhouse operations. The result shows that in the latter period, the SR values of the
control zones are similar to the values in the influence zones (p = 0.328, Table 14). In other words, and
considering also the results of Table 12, stocking rate is intensifying at much faster rates away from the
large slaughterhouses than closer to them.

Table 14. Results of Mann-Whitney test comparing the SRSL and SRCL in Amazonia.

Latter Period (Ha: SRSL = SRC

L)
SIF Code SRSL (Head/ha) Control Code L (Head/ha)
SRC
791 1.873 1 1.073
3348 1.240 2 1.554
1940 1.150 3 0.286
2583 1.423 4 1.504
2937 1.728 5 1.684
4149 1.902 6 1.588
4267 2.036 7 2.018
4333 1.821 8 1.453
Median 1.775 1.529
p 0.328 NS

NS Indicates not significant at 5% level.

Our results also demonstrate that the relationship between SR and ΔLU is not easily defined.
After the slaughterhouse start of operation in the Amazon, although ΔLU dropped everywhere, the
process of intensification did not start in the influence zones. Through a historical comparison between
the US and Brazil, Merry and Soares [18] suggested that Brazilian cattle ranching will intensify as a
result of economic conditions and conservation investments (reductions in capital and land subsidies)
rather than intensifying in order to produce conservation outputs. In addition, characteristics that
facilitate extensive ranching practices need to be discouraged or removed. The relatively easy process
of land acquisition—land grabbing and low land prices—accompanied by weak protection laws that
facilitates forest clearing for new pasture areas are the main obstacles of intensive ranching profitability,
and may continue to be so in the next years [10,40,41].
Finally, the main limitation of this work is related to three assumptions. First, as we assume the
zone of slaughterhouse influence extends up to 8 h travel time from a slaughterhouse, we may have
excluded pasture areas dedicated to the cow–calf segment of the market. This segment is the main

112
Sustainability 2018, 10, 3266

challenge on the pathway to achieving sustainable cattle ranching in Brazil, because it is not monitored
or tracked under the current cattle agreements [13]. In addition, nearly all cow–calf production
continues to be dependent on extensive grazing systems in the country [9].
Second, we may underestimate the area influenced by slaughterhouses, and therefore the
appropriate sizes of the influence and control zones. We do not consider variables such as cattle
availability, market access and transportation cost in the zone size estimates. Today, about 49% of
active slaughterhouses in Amazonia belong to companies that signed the TAC, corresponding to 70%
of slaughter capacity in the biome [19]. Therefore, the similarities observed between the control and
influence zones may indicate that small slaughterhouses, which are not considered in this analysis and
may be found inside some areas designated as control zones, may affect their supply areas in the same
way that large units do.
The third limitation is related to the assumption that only 12 selected slaughterhouses have
influence in their respective supply area. As observed in Figure 2, many large slaughterhouses are
near the selected ones and they may influence the variables analyzed along with the selected units.
We assumed here that the effect of these older slaughterhouses has not changed in time, and the main
effect measured is due to the slaughterhouses that started operations in the period of analyses. Only
two slaughterhouses do not have other large units near them: SIF 4333 in Amazonia and SIF 3047 in
the Cerrado (Figure 2). Although it is not possible to test statistically one slaughterhouse, SIF 4333 has
the same direction of change of the set of Amazonia plants for ΔLU, GE, PC and CC at all influence
zones (Table 4, Table 6, Table 8, and Table 10) and for SR at the 6 h and 8 h influence zone (Table 12).
Similar results are found for SIF 3047 when compared to the Cerrado set, except for ΔLU at the 2 h
influence zone. This is an indication of the effectiveness of this assumption.

5. Conclusions
This study investigated the influence of large slaughterhouses on five variables, two related to
environment impact (land use change rate and GHG emissions), and three related to cattle-ranching
intensification (protein from crops, calories from crops and stocking rate). The results indicate that the
changes observed inside the zones influenced by slaughterhouses cannot be attributed to the start of
slaughterhouse unit operation in either Amazonia or the Cerrado.
In the Amazon, the environmental impact variables we studied show the same pattern of
responses inside and outside the slaughterhouse influence zones—both moving towards reduced
environmental impact. The hypothesis that slaughterhouses are leverage points to reduce deforestation
and suppression of native Cerrado vegetation is not confirmed, leading us to believe that conservation
measures such as a strong monitoring system and more restrictive environmental policies are the
main promoters of conservation in Amazonia. In addition, the slaughterhouses seem to have no
effect on cattle-ranching intensification. The high stocking rates observed in the period before the
slaughterhouses’ start of operation indicate that large meatpackers prefer to set up their plants in areas
already well established and developed in the biome.
In the Cerrado, the responses of the environmental impact variables both inside and outside the
slaughterhouse influence zones indicate that there is considerable conservation work to be done in
the biome. The success of sustainable agriculture in the Cerrado still relies on the implementation
of conservation measures. In addition, the increase of PC, CC, and SR both inside and outside the
influence zones demonstrates that, in the Cerrado, cattle-ranching intensification is a reality, and it is
occurring independently of the presence of large slaughterhouses.
In conclusion, there is no evidence that large slaughterhouses have promoted either cattle-ranching
intensification or improvements in the sustainability of cattle-ranching activity in the Amazon and
Cerrado. The results of our study and the recent failures of some of the cattle agreements show
that leaning on slaughterhouses should not be considered a reliable strategy to achieve sustainable
beef production. According to Lambin et al. [42], zero-deforestation agreements signed by private
sectors may not be sufficient to reduce environmental impacts in commodities supply chain; public

113
Sustainability 2018, 10, 3266

and private policies need to complement and reinforce each other to disconnect the link between
cattle production and deforestation. In addition, to achieve intensification, it is necessary to improve
the ranchers’ access to technologies and capital [43,44], as there are still too many cattle farmers in
Amazonia and the Cerrado who are engaging in extensive ranching practices associated with low
income and high environmental damage.

Author Contributions: A.B.S. and M.H.C. contributed equally to the design of the research, the analysis of the
results and the writing of the manuscript.
Funding: This research was funded by CNPq—Conselho Nacional de Desenvolvimento Científico e Tecnológico
(process 134430/2015-8).
Conflicts of Interest: The authors declare no conflict of interest.

Appendix Table with All Abbreviations Used in the Text

ABBREVIATIONS
AGB Aboveground biomass
BGB Belowground biomass
Cadastro Ambiental Rural
CAR
(Rural Environmental Registry)
Cadastro Nacional de Pessoa Jurídica
CNPJ
(National Register of Legal Entities)
Sistema de Detecção de Desmatamento em Tempo Real
DETER
(System for the Detection of Deforestation in Real Time)
Departamento de Inspeção de Produtos de Origem Animal
DIPOA
(Department for Inspection of Animal Products)
GHG Greenhouse Gases
GWP Global Warming Potential
Instituto Brasileiro de Geografia e Estatística
IBGE
(Brazilian Institute of Geography and Statistics)
Instituto Nacional de Pesquisas Espaciais
INPE
(National Institute for Space Research)
IPCC Intergovernmental Panel on Climate Change
LULUCF Land Use, Land Use Change and Forestry
Ministério da Agricultura, Pecuária e Abastecimento
MAPA
(Brazilian Ministry of Agriculture, Livestock and Food Supply)
Acronym created from the first two letters of the states of Maranhão,
MATOPIBA
Tocantins, Piauí, and Bahia
NGOs Non-Governmental Organizations
Plano Nacional de Logística e Transporte
PNLT
(National Logistics and Transportation Plan)
Política Nacional sobre Mudanças no Clima
PNMC
(Brazil’s National Policy on Climate Change)
Projeto de Monitoramento da Floresta Amazônica Brasileira por Satélite
PRODES
(Program for Satellite Monitoring of the Brazilian Amazon Forest)

114
Sustainability 2018, 10, 3266

Appendix Biomass Map and Emissions from Enteric Fermentation

The biomass map of the historic vegetation for Amazonia and the Cerrado is presented in
Figure A1. The historic carbon content of native vegetation was 68.7 Pg-C for Amazonia and 10.1 Pg-C
for the Cerrado. Estimation of the historic vegetation is a complicated process, and results can vary
widely. Our estimate is comprehended in the range calculate by Leite et al. [45] for Amazonia (from
51.3 to 85.5 Pg-C); however, our estimate is about 53% less than the estimate for the Cerrado (from
13.8 to 28.8 Pg-C). The historic carbon content of native vegetation estimated in this study is different
from the values reported in Leite et al. [45] because different methodologies and values of carbon
stock were used to make the biomass maps. While Leite et al. [45] combined two maps of vegetation
types (RadamBrasil and IBGE [25]) and used the values for carbon stock in vegetation from the Second
National Communication of Brazil to the UNFCCC, we used the map from IBGE [25] and the data
from the Third National Communication.

Figure A1. Biomass map for past vegetation of Amazonia and the Cerrado.

Another result is the CH4 emissions from enteric fermentation. Between 2000 and 2013, the
emissions from beef cattle increased in both biomes. Total methane emission by the two biomes in
this period amounted to 2.9 Pg-CO2e , about 54% of the total emitted in the country (5.3 Pg-CO2e [2]).
Emissions in Amazonia increased about 80% (from 41.7 Tg-CO2e in 2000 to 77.5 Tg-CO2e in 2013).
In the Cerrado, emissions increased about 0.09% (from 82.5 Tg-CO2e in 2000 to 90.5 Tg-CO2e in 2013).
The increase was bigger in the Amazon than in the Cerrado because of the great increase in number of
cattle that occurred in this period.
Our estimates for methane emissions are very similar to other data. According to
Azevedo et al. [2], for the states of the Amazon biome, the total amount of methane emitted by enteric
fermentation from beef cattle was 1.0 Pg-CO2e for the period, while our estimate was 0.9 Pg-CO2e .

115
Sustainability 2018, 10, 3266

For the states of the Cerrado, Azevedo et al. [2] reported total methane emissions of 2.0 Pg-CO2 -eq
for the period, about 35% greater than our estimate of about 1.3 Pg-CO2 -eq. These Cerrado estimates
differ because we consider the actual geographic limits of the biome, while the Azevedo et al. [2] value
includes total emissions for all Cerrado states, irrespective of how much area within the states is part
of the Cerrado biome.

References
1. Ministério da Ciência, Tecnologia e Inovação. Third National Communication of Brazil to the United Nations
Framework Convention on Climate Change; Ministério da Ciência, Tecnologia e Inovação: Brasilia, Brazil, 2016;
Volume III, ISBN 9788588063198.
2. De Azevedo, T.R.; Costa Junior, C.; Brandão Junior, A.; Cremer, M.D.S.; Piatto, M.; Tsai, D.S.; Barreto, P.;
Martins, H.; Sales, M.; Galuchi, T.; et al. SEEG initiative estimates of Brazilian greenhouse gas emissions
from 1970 to 2015. Sci. Data 2018, 5, 1–43. [CrossRef] [PubMed]
3. Cohn, A.S.; Mosnier, A.; Havlík, P.; Valin, H.; Herrero, M.; Schmid, E.; O’Hare, M.; Obersteiner, M.
Cattle ranching intensification in Brazil can reduce global greenhouse gas emissions by sparing land from
deforestation. Proc. Natl. Acad. Sci. USA 2014, 111, 7236–7241. [CrossRef] [PubMed]
4. Strassburg, B.B.N.; Latawiec, A.E.; Barioni, L.G.; Nobre, C.A.; da Silva, V.P.; Valentim, J.F.; Vianna, M.;
Assad, E.D. When enough should be enough: Improving the use of current agricultural lands could meet
production demands and spare natural habitats in Brazil. Glob. Environ. Chang. 2014, 28, 84–97. [CrossRef]
5. Crosson, P.; Shalloo, L.; O’Brien, D.; Lanigan, G.J.; Foley, P.A.; Boland, T.M.; Kenny, D.A. A review of whole
farm systems models of greenhouse gas emissions from beef and dairy cattle production systems. Anim. Feed
Sci. Technol. 2011, 166–167, 29–45. [CrossRef]
6. De Oliveira Silva, R.; Barioni, L.G.; Hall, J.A.J.; Matsuura, M.F.; Zanett Albertini, T.; Fernandes, F.A.; Moran, D.
Increasing beef production could lower greenhouse gas emissions in Brazil if decoupled from deforestation.
Nat. Clim. Chang. 2016, 6, 493–497. [CrossRef]
7. Mazzetto, A.M.; Feigl, B.J.; Schils, R.L.M.; Cerri, C.E.P.; Cerri, C.C. Improved pasture and herd management
to reduce greenhouse gas emissions from a Brazilian beef production system. Livest. Sci. 2015, 175, 101–112.
[CrossRef]
8. Palermo, G.C.; D’Avignon, A.L.D.A.; Freitas, M.A.V. Reduction of emissions from Brazilian cattle raising
and the generation of energy: Intensification and confinement potentials. Energy Policy 2014, 68, 28–38.
[CrossRef]
9. Ferraz, J.B.S.; de Felício, P.E. Production systems—An example from Brazil. Meat Sci. 2010, 84, 238–243.
[CrossRef] [PubMed]
10. Bowman, M.S.; Soares-Filho, B.S.; Merry, F.D.; Nepstad, D.C.; Rodrigues, H.; Almeida, O.T. Persistence of
cattle ranching in the Brazilian Amazon: A spatial analysis of the rationale for beef production. Land Use
Policy 2012, 29, 558–568. [CrossRef]
11. Dias, L.C.P.; Pimenta, F.M.; Santos, A.B.; Costa, M.H.; Ladle, R.J. Patterns of land use, extensification, and
intensification of Brazilian agriculture. Glob. Chang. Biol. 2016, 22, 2887–2903. [CrossRef] [PubMed]
12. Barreto, P.; Pereira, R.; Arima, E. A Pecuária e o Desmatamento na Amazônia na era das Mudanças Climáticas;
Instituto do Homem e Meio Ambiente da Amazônia: Belém, Brazil, 2008; ISBN 9788586212260.
13. Gibbs, H.K.; Munger, J.; L’Roe, J.; Barreto, P.; Pereira, R.; Christie, M.; Amaral, T.; Walker, N.F. Did ranchers
and slaughterhouses respond to zero-deforestation agreements in the Brazilian Amazon? Conserv. Lett. 2016,
9, 32–42. [CrossRef]
14. Greenpeace. Eating up the Amazon. Available online: http://www.greenpeace.org/usa/research/eating-
up-the-amazon/ (accessed on 16 May 2016).
15. Greenpeace. Slaughtering the Amazon. Available online: http://www.greenpeace.org/international/en/
publications/reports/slaughtering-the-amazon/ (accessed on 16 May 2016).
16. Walker, N.; Patel, S.; Kalif, K. From Amazon pasture to the high street: Deforestation and the Brazilian cattle
product supply chain. Trop. Conserv. Sci. 2013, 6, 446–467. [CrossRef]
17. Garcia, E.; Filho, F.S.V.R.; Mallmann, G.M.; Fonseca, F. Costs, benefits and challenges of sustainable livestock
intensification in a major deforestation frontier in the Brazilian Amazon. Sustainability 2017, 9, 158. [CrossRef]

116
Sustainability 2018, 10, 3266

18. Merry, F.; Soares-Filho, B. Will intensification of beef production deliver conservation outcomes in the
Brazilian Amazon? Elem. Sci. Anth. 2017, 5, 1–12. [CrossRef]
19. Barreto, P.; Pereira, R.; Brandão, A., Jr.; Baima, S. Os Frigoríficos vão Ajudar a Zerar o Desmatamento da Amazônia?
Imazon: Belém, Brazil, 2017; ISBN 9788586212949.
20. Alves-Pinto, H.N.; Newton, P.; Pinto, L.F.G. Certifying Sustainability: Opportunities and Challenges for the
Cattle Supply Chain in Brazil; Research Program on Climate Change; Agriculture and Food Security (CCAFS):
Copenhagen, Denmark, 2010; pp. 1–8.
21. Zu Ermgassen, E.K.H.J.; de Alcântara, M.P.; Balmford, A.; Barioni, L.; Neto, F.B.; Bettarello, M.M.F.; de
Brito, G.; Carrero, G.C.; Florence, E.D.A.S.; Garcia, E.; et al. Results from on-the-ground efforts to promote
sustainable cattle ranching in the Brazilian Amazon. Sustainability 2018, 10, 1301. [CrossRef]
22. Barreto, P.; Silva, D. Will cattle ranching continue to drive deforestation in the Brazilian Amazon?
In Environment and Natural Resources Management in Developing and Transition Economies; Centre of Studies
and Research on International Development from the University of Auvergne: Clermont Ferrand, France,
2010; pp. 1–23.
23. Hansen, M.C.; Potapov, P.V.; Moore, R.; Hancher, M.; Turubanova, S.A.; Tyukavina, A.; Thau, D.;
Stehman, S.V.; Goetz, S.J.; Loveland, T.R.; et al. High-Resolution Global Maps of 21st-Century Forest
Cover Change. Science 2013, 342, 850–853. [CrossRef] [PubMed]
24. Bustamante, M.; Santos, M.M.D.O.; Shimbo, J.Z.; Cantinho, R.Z.; Mello, T.D.R.B.D.; Oliveira, P.V.D.C.;
Cunha, P.W.P.D.M.; Martins, F.D.S.R.V.; Aguiar, A.P.D.; Ometto, J. Emissões do Setor de uso da Terra, Mudança
do uso da Terra e Florestas: Relatório de Referência; Ministério da Ciência, Tecnologia e Inovação: Brasíla, Brazil,
2015; p. 343.
25. IBGE. Mapa de Vegetação. 2004. Available online: https://mapas.ibge.gov.br/tematicos/vegetacao
(accessed on 13 February 2016).
26. Berndt, A.; Lemes, A.P.; Romero, L.A.; Sakamoto, L.S.; Lima, M.A. De Emissões de Metano por Fermentação
Entérica e Manejo de Dejetos de Animais: Relatório de Referência; EMBRAPA; Ministério da Ciência, Tecnologia e
Inovação: Brasília, Brazil, 2015; p. 150.
27. IPCC. IPCC Guidelines for National Greenhouse Gas Inventories. 2006. Available online: https://www.
ipcc-nggip.iges.or.jp/public/2006gl/ (accessed on 1 April 2016).
28. Cardoso, E.G. Engorda de Bovinos em Confinamento (Aspectos Gerais). Embrapa, 1996. Available
online: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/317195/engorda-de-bovinos-em-
confinamento-aspectos-gerais (accessed on 15 April 2018).
29. Da Costa, M.J.R.P.; Quintiliano, M.H.; Tseimazides, S.P. Boas Praticas de Manejo—Transporte; MAPA/ACS:
Brasília, Brazil, 2013; ISBN 9788579910715.
30. Confederação Nacional do Transporte. Anuário CNT do Transporte—Estatísticas Consolidadas. Available
online: http://anuariodotransporte.cnt.org.br/2017/ (accessed on 20 April 2018).
31. Boucher, D. How Brazil has dramatically reduced tropical deforestation. Solutions 2014, 5, 65–75.
32. Kastens, J.H.; Brown, J.C.; Coutinho, A.C.; Bishop, C.R.; Esquerdo, J.C.D.M. Soy moratorium impacts on
soybean and deforestation dynamics in Mato Grosso, Brazil. PLoS ONE 2017, 12, 0176168. [CrossRef]
[PubMed]
33. Nepstad, D.; McGrath, D.; Stickler, C.; Alencar, A.; Azevedo, A.; Swette, B.; Bezerra, T.; DiGiano, M.;
Shimada, J.; da Motta, R.S.; et al. Slowing Amazon deforestation through public policy and interventions in
beef and soy supply chains. Science 2014, 344, 1118–1123. [CrossRef] [PubMed]
34. Soares-Filho, B.; Rajao, R.; Macedo, M.; Carneiro, A.; Costa, W.; Coe, M.; Rodrigues, H.; Alencar, A. Cracking
Brazil’s forest code. Science 2014, 344, 363–364. [CrossRef] [PubMed]
35. Gibbs, H.K.; Rausch, L.; Munger, J.; Schelly, I.; Morton, D.C.; Noojipady, P.; Soares-Filho, B.; Barreto, P.;
Micol, L.; Walker, N.F. Brazil’s soy moratorium. Science 2015, 347, 377–378. [CrossRef] [PubMed]
36. INPE. Instituto Nacional de Pesquisas Espaciais 2013. Available online: http://www.inpe.br/ (accessed on
20 December 2017).
37. Macedo, M.N.; DeFries, R.S.; Morton, D.C.; Stickler, C.M.; Galford, G.L.; Shimabukuro, Y.E. Decoupling of
deforestation and soy production in the southern Amazon during the late 2000s. Proc. Natl. Acad. Sci. USA
2012, 109, 1341–1346. [CrossRef] [PubMed]
38. IBAMA Projeto de Monitoramento dos Biomas Brasileiros via Satélite (PMDBBS). Available online: http:
//siscom.ibama.gov.br/monitora_biomas/ (accessed on 20 December 2017).

117
Sustainability 2018, 10, 3266

39. Bellantonio, M.; Hurowitz, G.; GrØnlud, L.; Yousefi, A. Ultimate Mystery Meat. Available online:
http://www.mightyearth.org/mysterymeat/ (accessed on 16 October 2017).
40. Cardoso, D.; Brito, B.; Baima, S.; Siqueira, V. O Estado da Amazônia Potencial de Arrecadação Financeira com a
Regularização Fundiária no Pará; Imazon: Belém, Brazil, 2018; p. 14.
41. Azevedo-Ramos, C.; Silva, J.N.M.; Merry, F. The evolution of Brazilian forest concessions. Elem. Sci. Anth.
2015, 3, 000048. [CrossRef]
42. Lambin, E.F.; Gibbs, H.K.; Heilmayr, R.; Carlson, K.M.; Fleck, L.C.; Garrett, R.D.; de Waroux, Y.L.P.;
McDermott, C.L.; McLaughlin, D.; Newton, P.; et al. The role of supply-chain initiatives in reducing
deforestation. Nat. Clim. Chang. 2018, 8, 109–116. [CrossRef]
43. Monzoni, M.; Vendramini, A.; Rocha, F.C.; Peirão, P.; Campanili, M.; Sobreiro, A.; Monteiro, A. Análise dos
Recursos do Programa ABC Safra 2016/17; Centro de Estudos em Sustentabilidade da Fundação Getúlio Vargas
(GVces): São Paulo, Brazil, 2017; pp. 1–36.
44. Latawiec, A.E.; Strassburg, B.B.N.; Valentim, J.F.; Ramos, F.; Alves-Pinto, H.N. Intensification of cattle
ranching production systems: Socioeconomic and environmental synergies and risks in Brazil. Animal 2014,
8, 1255–1263. [CrossRef] [PubMed]
45. Leite, C.C.; Costa, M.H.; Soares-Filho, B.S.; Hissa, L.D.B.V. Historical land use change and associated carbon
emissions in Brazil from 1940 to 1995. Glob. Biogeochem. Cycles 2012, 26, 1–13. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

118
 sustainability

Article
Greenhouse Gas Emissions from Beef Grazing
Systems in Semi-Arid Rangelands of
Central Argentina
María I. Nieto 1 , Olivia Barrantes 2,3, * , Liliana Privitello 4 and Ramón Reiné 5
1 Instituto Nacional de Tecnología Agropecuaria (INTA), Estación Experimental Agropecuaria Catamarca,
Ruta 33 Km 4 (4705), Sumalao, 4705 Catamarca, Argentina; [email protected]
2 Departamento de Ciencias Agrarias y del Medio Natural, Facultad de Veterinaria, Universidad de Zaragoza,
Miguel Servet 177, 50013 Zaragoza, Spain
3 Instituto Agroalimentario de Aragón -IA2- (CITA-Universidad de Zaragoza), 50013 Zaragoza, Spain
4 Departamento de Ciencias Agropecuarias, Facultad de Ingeniería y Ciencias Agropecuarias,
Universidad Nacional de San Luis, Av. 25 de Mayo 384, Villa Mercedes, 5730 San Luis, Argentina;
[email protected]
5 Departamento de Ciencias Agrarias y del Medio Natural, Escuela Politécnica Superior, Universidad de
Zaragoza, Carretera de Cuarte s/n, 22071 Huesca, Spain; [email protected]
* Correspondence: [email protected]; Tel.: +34-976-761-596

Received: 30 September 2018; Accepted: 12 November 2018; Published: 16 November 2018

Abstract: The livestock sector can be a major contributor to the mitigation of greenhouse gas (GHG)
emissions. Within the sector, beef production produces the largest proportion of the livestock
sector’s direct emissions. The objective of this study was to assess the on-farm GHG emissions in
semi-arid rangelands in Argentina and to identify the relationship between emissions and current
farm management practices. A survey recorded detailed information on farm management and
characteristics. Assessments of GHG emissions were based on the Intergovernmental Panel on
Climate Change (IPCC) Tier 2 protocols. The relationship between farm management and GHG
emissions were identified using general linear models. Cluster analysis was used to identify groups of
farms that differed from others in emissions and farm characteristics. Emissions per product sold were
low on farms that had improved livestock care management, rotational grazing, received technical
advice, and had high animal and land productivities. Emissions per hectare of farmland were low
on farms that had low stocking rates, a low number of grazing paddocks, little or no land dedicated
to improved pastures and forage crops, and low land productivity. Our results suggest that the
implementation of realistic, relatively easy-to-adopt farming management practices has considerable
potential for mitigating the GHG emissions in the semi-arid rangelands of central Argentina.

Keywords: livestock care management; rotational/continuous grazing; technical advice; stocking

rate; functional units

1. Introduction
Livestock production is an important source of greenhouse gas (GHG) emissions worldwide.
The livestock sector contributes 14.5% of global GHG emissions [1]. Since the human population is
expected to increase from 7.2 to 9.6 billion by 2050 [2], together with the improvement of standard
of living, there is an increasing demand for livestock products [3], which are expected to double by
the mid-21st century [4]. The livestock sector will have to be a major contributor in the mitigation of
GHG emissions and in the improvement of global food security [5]. Within the sector, beef production
contributes the majority of emissions, producing 41% of the livestock sector’s direct emissions [6].
Methane (CH4 ) and nitrous oxide (N2 O) are the largest contributors to global livestock emissions in

Sustainability 2018, 10, 4228; doi:10.3390/su10114228 119 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 4228

CO2 equivalent (CO2 e) per year [1]. In countries where pastoral agriculture is the dominant sector,
CH4 and N2 O emissions contribute up to 50% of the total GHG emissions [7]. Due to the negative
relation between the efficiency of production and GHG emissions per output produced, the greatest
mitigation potential lies in ruminant systems that operate with a low productivity (e.g., in South Asia,
Latin America, the Caribbean, and Africa) [1].
Argentina is a major world beef producer. It is the sixth largest beef producer in the world [8]
and the ninth largest beef exporter [9]. The meat chain generates around 4% of the total jobs in the
country [9]. Argentina and four other Latin American main beef exporters plan to increase meat
production in response to the forecasted growth in international markets [10]. Of the 156.94 Mt CO2 e
emitted by the Argentinean sector relating to ‘Agriculture, Forestry and other land uses’, livestock
directly accounts for 54 Mt CO2 e, produced by enteric fermentation (of which beef accounts for 83%);
20.26 MtCO2 e are produced by manure deposition on pastures (76% from beef); and 2.14 MtCO2 e are
produced by manure management (83% from beef) [11]. Thus, methane emitted by enteric fermentation
is especially important. In 2008, methane emissions from domestic ruminants in Argentina was the sixth
highest in the world, and the per capita rate was one of the highest [12]. Rearte and Pordomingo [10]
indicated there are ample opportunities to reduce methane emissions per unit of product in Argentina
and other temperate regions of Latin America, such as Uruguay.
The GHG emissions of a product can be expressed as kg of CO2 e per kg of product, or it can be
expressed as kg of CO2 e per unit of area (ha) of the production system, depending on the perspective
(that of the consumer vs. that of the producer) [13–15] and product perspective vs. an IPCC inventory
perspective [16,17]. From a ‘product perspective’, Casey and Holden [16] suggested that it is necessary
to choose a functional unit (FU, kg of product vs. land area) of the function that the system delivers.
However, for studies that intend to inform national GHG inventory reports, an FU coupled with land
area is necessary [16,17]. Finally, environmental impacts per unit of product are more closely linked
with the assessment of global issues, such as climate change [15,18], while assessing an environmental
impact per hectare of land is considered a more local or regional issue, such as soil erosion, water
eutrophication, or acidification [18]. Some studies have shown that the use of different FUs can produce
contradictory results in assessing GHG emissions [13,14,16], illustrating the potential trade-off between
carbon efficiencies per unit of product and per unit of land. Nevertheless, several studies suggest that
the mitigation of emissions per unit of product and per unit of land area can be reconciled [14,16].
Casey and Holden [16], Halberg et al. [18] and Veysset et al. [19] suggested that product-based and
land area-based indicators should be used to characterize the environmental impacts caused by
food production.
Many studies have assessed mitigation strategies for reducing GHG emission intensity in
terms of emissions per unit of animal product in several ruminant livestock farming systems
worldwide, which have been reviewed extensively [1,5,20–27]. The mitigation strategies that reduce
emission intensity by increasing herd productivity through improved animal husbandry practices
(e.g., animal feeding, genetics, health, fertility, and the overall management of the animal operations)
can be important in low–input ruminant systems [12,22] and have a greater mitigation potential in
development than they do in developed economies [22].
In Argentina, >70% of the beef is produced in pasture-based grazing systems [10], mostly in
extensive conditions [12]. As the opportunity for soybeans and cereal grains became structural to
Argentinean agriculture, livestock businesses were displaced towards less productive, marginal
lands [10,28]. Eight percent of beef production is in the semi-arid Central Region (18% of the
country) [29]. Rangeland native grasslands are the main source of feed for cow-calf livestock systems,
which constitute an important economic sector in the region [30]. Rangelands are the world’s most
common land type [31], and they provide the livelihoods for many vulnerable communities throughout
the world [32]. Their relevance is linked to their multifunctional nature and provision of ecosystem
services [33]. Extensively managed livestock production is the most sustainable and common form
of agriculture on rangelands [33]. Global demand for livestock products will increase the pressure

120
Sustainability 2018, 10, 4228

on rangelands, which are experiencing high degradation and losses in biodiversity worldwide [34],
especially in arid and semi-arid grasslands in developing countries [33].
Identifying the relationship between GHG emissions, farm management and system productivity
can help livestock producers improve operations, where productivity can be improved considerably
by implementing simple management practices [35]. Furthermore, in the transition to sustainable
livestock production, assessments of mitigation measures that have been tailored to the location
and livestock production system in use are needed [5,14]. Our study assessed commercial farms
that were representative of the extensive beef systems, based on natural rangelands in the San Luis
Province, which is typical of the semi-arid Central Region of Argentina [28]. Beef cattle stocks have
increased in San Luis because of the displacement of livestock into semi-arid marginal areas [36] and
incipient intensification has been reported [28]. The main objective was to assess GHG emissions from
representative farms in order to identify realistic farming practices that will favor low GHG emissions.
Specifically, we (i) estimated the CH4 and N2 O on-farm livestock emission intensity based on two
functional units: product-based (kg CO2 e per total live weight sold) and area-based (kg CO2 e per land
area used); (ii) identified farm attributes and management practices that were associated with low
emission intensities; and (iii) assessed the implications of using each of the two functional units in
identifying the farming practices that minimize GHG emissions.

2. Materials and Methods

The study was conducted in a 4160-km2 area in the San Luis province, Central Region, Argentina
(center of the study area: 34◦ 17 22.46 S; 66◦ 25 40.89 W), where an extensive cow-calf system, based
on year-round, open-air grazing, is the main land use. The climate is semi-arid, and the annual
precipitation ranges from 350 to 500 mm. The average daily temperature ranges from 8.5 ◦ C (coldest
month) to 23 ◦ C (warmest month) [37]. The soils are shallow, poor in organic matter, have low
water retention capacity, and low-medium productivity [38]. The climate and soil conditions are
unsuited to croplands, and rangeland native grasslands are the main source of feed for livestock [30].
Natural vegetation consists of two main types [39]: (i) a woodland-shrubland mixture dominated
by legume trees (Prosopis flexuosa and Geoffroea decorticans) and shrubs (Larrea divaricata); and (ii)
grass-dominated steppes of Nassella tenuis, Piptochaetium napostaense, Poa ligularis and Poa lanuginose,
and small scattered woodlands of legume trees (mainly G. decorticans). Most of the cattle are Hereford,
Aberdeen Angus, or crossbreeds of the two, although some farms also have Creole [40]. A low
productivity and potential improvement of the farm system have previously been reported in the
region [10].
In 2014, 30 of the 67 beef cattle farms in the study area were surveyed. The farms were
representative of the region based on earlier studies [30]. The survey, recorded in a structured
questionnaire, collected detailed information about the size and structure of the farm, livestock
management, infrastructures, productivity, as well as the ages and levels of education of the producer
and the labor, referred to a one-year production cycle. With that information, a characterization of the
farms was obtained, and variables were calculated, which were used in the analysis.
The general characteristics of the farms are detailed in Table 1. Seven percent of the farmers did
not have any type of education, 61% had a primary or secondary education, and 32% had higher
education. Half of the farms surveyed had salaried employees. In addition to natural grassland areas,
23% of the farms improved grasslands by introducing grasses, such as Eragrostis curvula, Digitaria
eriantha, and Panicum coloratm cv. verde, and 17% had annual forage crops, such as maize (Zea mays),
sorghum (Sorghum vulgare), rye (Secale cereale) with melilotus (Melilotus albus), and oats (Avena sativa),
although in both cases, the areas were much smaller than the natural pastures (4% and 2% of the total
land on average, respectively, Table 1). The annual forage crops are seeded if there have been enough
rains; they are ‘low-input’ crops, which are not mowed but only grazed, and farmers generally do not
use pesticides or chemical fertilizers. Half of the farmers purchased small amounts of maize, alfalfa or
mineral complements, only in winter in critical years and not always for feeding all animal categories.

121
Sustainability 2018, 10, 4228

Three types of production systems were observed: (i) cow-calf (CC) systems (60% of the farms), where
calves are sold at weaning; (ii) backgrounding (BG) systems (10%) (i.e., farmers purchase weaned
calves that are sold once they are fattened); and (iii) cow-calf + backgrounding (CCBG) systems (30%).
The calves are weaned at 6 months at 130–150 kg of live weight (LW) and sold fattened at 15 months
(280–300 kg LW). On the CC and CCBG farms, the reproductive system was either (i) year-round
mating (44% of the farms), or (ii) seasonal. Only 7% of farms employed artificial insemination. On the
farms, water was collected in artificial dams by drilling, extraction from wells and, to a lesser extent,
using natural streams.

Table 1. General characteristics of the beef cattle farms in San Luis province, central Argentina.

Variable Mean s.d. Min Max

Socio-economic data
Age (years) 56 11.3 34 75
+ Hired labor (WU/LU) (×10−3 ) 0.7 0.8 0 2.5
Land use
+
Total land area (ha) 3598 4706 67 23,400
+ Land area used for native pastures (%) 95 14 33 100
+ Land area used for improved pastures (%) 4 13 0 67
Land area for annual forage crops (%) 2 6 0 29
Beef cattle
+ Total Livestock Units 1 (LU) 337 399 17 1856
Mortality rate (%) 6.7 11.1 0.6 50.0
Stocking rate (LU/ha) 0.13 0.09 0.02 0.46
Grazing infrastructures
Water reservoirs per total land/ha (×10−3 ) 2.8 3.2 0.3 14.9
Water reservoirs/LU (×10−3 ) 25 21 4 89
+ Grazing paddocks/ha (×10−3 ) 3.7 4.5 0.6 19.6
System productivity
Average LW of livestock (kg) 283 50 195 399
Weaning rate 2 (%) 65 17 26 95
+ Land productivity (kg LW sold/ha) 18.3 20.4 1.1 93.8
+ Animal productivity (kg LW sold/LU) 138 91 53 337
s.d., standard deviation; Min and Max, minimum and maximum values (n = 30 farms); WU, work units; LU,
livestock units; LW, live weight. + Variables used for the typification of the beef cattle farms. 1 Livestock units were
calculated based on Cocimano et al. [41]. 2 n = 27 (remaining three farms are backgrounding systems; they do not
have breeding).

GHG emissions were estimated on-farm, based on the CH4 emissions from cattle enteric
fermentation and N2 O emissions from the managed soils used by grazing animals. Animals graze
year-round, and manure is not managed, which is consistent with the Intergovernmental Panel on
Climate Change (IPCC) [42]. No animal housing was involved, and crops and imported feeds were
not relevant in the study area. CO2 emissions from infrastructure, energy used for crops, and off-farm
GHG emissions were not included in this study. Therefore, we focused on the relevant on-farm
GHG emissions, as affected by the farm management practices. GHG emissions were expressed
as CO2 equivalents (CO2 e) for a time horizon of 100 years: CH4 kg × 25 and N2 O kg × 298 [43].
Emissions were expressed as kgCO2 e per kg LW sold (sum of weaned calves and culled cows), and
per hectare (ha) of farmland.
Assessments of GHG emissions were based on the IPCC Tier 2 protocols [42]. Appendix A shows
the IPCC (2006) equations used in the calculations. Further updates of IPCC (2006) protocols did not
affect those equations. Enteric CH4 was estimated for each category of cattle on the farm: cow, weaned
calf, replacement heifer, bull and steer.

122
Sustainability 2018, 10, 4228

Estimates of the gross energy (GE) intake of the animals were calculated based on the net energy
(NE) requirements for maintenance, activity, growth, pregnancy and lactation. Enteric emissions were
estimated based on GE intake and using methane conversion factors (Ym). We refined Ym calculations
using the Cambra-López et al. (2008) [44] equation: Ym = −0.0038*DE2 + 0.351*DE-0.8111, where
DE is feed digestibility, expressed as a percentage of the GE of the feed. DE was estimated based on
earlier studies on the quality of the pastures in the study area [45], percentage of land with annual
forage crops, and the opinions of local experts of the ‘Estación Experimental Agropecuaria San Luis’
del ‘Instituto Nacional de Tecnología Agropecuaria’ (INTA). The average DE was 58% (range = 52–60;
SD = 1.3), and the average Ym was 6.7% (range = 6.5–7.1; SD = 0.12).
N2 O emissions from managed soils were calculated based on the N deposited on pastures by
grazing animals (urine and dung). The amount of N deposited on the pasture by each cattle type
while grazing was estimated based on the number of animals, feed intake, pasture N content, and N
retention of the animals, following IPCC [42] and the National Research Council [46].
Two analyses were conducted: statistical models that described GHG emissions and
cluster analysis, identifying homogeneous groups of farms that differed in emissions and
management practices.
The relationship between farm management practices and GHG emission was investigated
using generalized linear models (GLM) [47], with the assumption that the data followed a Tweedie
distribution, and a logarithmic link function. The dependent variable was CO2 e emissions, which was
expressed as either (a) per kg of LW sold or (b) per hectare of land.
A set of explanatory variables was used for the models of each of the two dependent variables.
The values of all explanatory variables (nominal, ordinal, or continuous) were transformed
to 0–1 values and included as ‘factors’ (categorical predictors with values 0–1) in the models.
Nominal variables included feed purchase (0, no; 1, yes); the reproductive management of the
livestock (0, year-round mating; 1, seasonal mating); technical advice (0, no; 1, yes); type of production
system [0, cow-calf (CC); 1, cow-calf + backgrounding (CCBG)]; and grazing system (0, continuous;
1, rotational). For the ordinal and continuous variables, the scoring criteria were based on the
median (values ≤ median = 0; values > median = 1), except for the land area used for introduced
pastures or annual forage crops. Ordinal variables included water reservoirs per total land (0,
low; 1, moderate; median = 16.7 × 10−4 water reservoirs/ha); grazing paddocks per total land
(0, low; 1, moderate; median = 16 × 10−4 grazing paddocks/ha); and livestock care controls (0,
poor = three or fewer types of controls; 1, good = four to six types of controls; median = 3 controls).
The types of livestock care controls were body condition, teeth examination, rectal palpation/ecography,
parasite control, reproductive vaccine, and bull review control. Continuous variables included
land area used for introduced pastures or annual forage crops (0, null/very low if area ≤ 4%; 1,
low/moderate if area > 4%), average live weight of livestock (0, low; 1, moderate; median = 292 kg),
cows-to-total animals rate (0, low; 1, moderate; median = 55%), average weight of sold calf (0, low;
1, moderate; median = 204 kg), mortality rate (0, low; 1, moderate; median = 2.6%), stocking rate (0,
low; 1, moderate; median = 0.10 LU/ha), weaning rate (0, low; 1, moderate; median = 66.5%), land
productivity (0, low; 1, moderate; median = 9.2 kg LW sold/ha), and animal productivity (0, low; 1,
moderate; median = 100 kg LW sold/LU).
Prior to the GLM analysis, an exploratory analysis was conducted, based on the Mann–Whitney
test, to identify the independent effects of variables on GHG emissions, and a Spearman’s
non-parametric test was used to identify co-linearity among variables. Only non-correlated variables
(rs < 0.38, p > 0.05) were included in a given GLM. Backgrounding farms were excluded from the
analysis because they do not have a breeding herd.
Several analyses were performed based on all possible combinations of non-correlated variables
and removing the non-significant explanatory variables one at a time (variables that did not
reach p < 0.05 in a Wald’s Chi-square test) until the final models only contained significant
explanatory variables.

123
Sustainability 2018, 10, 4228

Only models that were significant (p < 0.05) based on an omnibus test were included in the
analyses. The resultant models were defined as:

LnE = α + β 1 var1 + β 2 var2 + . . . + β i vari ,

where E = CO2 e emission, the first term ‘α’ contains the regression intercept, and the remaining terms
include the variables used in the model. The model indicates the partial regression β coefficients,
which indicate the weights of the variables 1, 2, . . . , i in the model when the variable is ‘0’. Thus, if β
is > 0, E and the variable (level ‘0’) are positively correlated, and if β is < 0, E and the variable (level ‘0’)
are negatively correlated. If the variable is ‘1’, the model takes the reference value (β = 0 and, hence,
LnE = α). Emissions are calculated as:

E = eα ·e β1 var1 ·e β2 var2 · . . . ·e βi vari

The statistical significance of the coefficients of individual variables in the models was tested
using Wald’s Chi-square test. Significant interaction effects were not detected. To express the main
effects in each model, the estimated marginal means were calculated. For all possible combinations
of non-correlated variables in the models, a model fit was evaluated based on Akaike’s information
criterion for finite samples (AICc) [48]. ΔAICc was calculated as: ΔAICc = AICci − AICcmin , for i = 1,
2, . . . , R, where AICcmin denotes the minimum of the AICc values for the R models [49]. Models that
had the lowest AICc were selected as the best models within a set of models that included the same set
of variables [48]. Models with ΔAICc < 7 were considered plausible, and models with ΔAICc > 11 were
discarded [49]. The explained deviance reflected the contributions of significant individual explanatory
variables to the model as follows: D2 = (D0 − Dmodel )/D0 , where D0 is the deviance of the null model
(intercept only), and Dmodel is the deviance of the analyzed model [50]. The contribution of each
explanatory variable was estimated based on the change in D2 after the variable was deleted from the
model divided by the total explained deviance [51], which is expressed here as ‘D2 change on deletion’
(%DCD). As the values of the variables were 0 or 1, standardization of the explanatory variables was
not conducted. The statistical significance of the independent effects of each management variable on
GHG emissions was assessed based on Spearman’s correlation non-parametric tests.
For the typification of the farms, 7 continuous and 4 discrete variables were selected. To identify
the main factors (eigenvalues > 1) that characterized the changes observed, 11 variables were
subjected to principal component analysis (PCA), with varimax rotation. The Bartlett sphericity
test and a Kaiser–Meyer–Olkin (KMO) test for sampling adequacy were used to validate the sampling.
To identify a typology of the farms, we subjected the main factors of the PCA to a hierarchical cluster
analysis (CA), with a squared Euclidean distance and Ward’s aggregation method. In that way, five
groups of farms were identified. To validate the results, we used a non-parametric Kruskal–Wallis test,
known as ‘analysis of variance by ranges’ [52], which verifies which continuous variables, either those
used in the PCA-CA (7 variables) or not (10 variables), are significant in explaining the differences
between the groups. To identify which groups differ according to each continuous variable, we used
the non-parametric Dunn–Bonferroni post-hoc test. To identify differences between groups for the
discrete variables, we used the Pearson’s chi-square test. The testing of variables not included in the
CA is known as ‘criterion validity’ [53] and has been used to characterize livestock farms [54].
The statistical analyses were performed using IBM SPSS Advanced Statistics software ver. 22 [55].

3. Results

3.1. Farm Greenhouse Gas (GHG) Emissions

Among the beef farms in the San Luis province, central Argentina, the mean GHG emission
intensity was 19.6 kg CO2 e/kg LW sold, but varied widely (range = 6.2–39.7). Backgrounding (BG)
farms produced fewer emissions than did cow-calf (CC) farms, and mixed CCBG farms produced

124
Sustainability 2018, 10, 4228

average emissions. On a farm-area basis, the average emission rate was 261 kg CO2 e/ha (range = 26 to
1042), which did not differ significantly among types of production systems (Table 2).

Table 2. Farm greenhouse gas emissions of the beef cattle farms in San Luis province, central Argentina.

Farm Greenhouse
Gases Emission Production System Mean 1 s.d. Min Max n
Intensity
Cow-calf 23.6 b 7.3 12.4 39.7 18
Backgrounding 6.9 a 1.1 6.2 8.1 3
kg CO2 e/kg LW sold
Cow-calf + Backgrounding 15.7 ab 6.3 7.0 22.6 9
Overall 19.6 8.6 6.2 39.7 30
Cow-calf 243 225 26 1042 18
Backgrounding 345 70 270 409 3
kg CO2 e/ha
Cow-calf + Backgrounding 269 200 83 671 9
Overall 261 205 26 1042 30
s.d., standard deviation; Min and Max, minimum and maximum values; LW, live weight. 1 Different letters in the
same column indicate significant differences between production system groups (p = 0.002). Kruskal–Wallis test.

3.2. Effects of Farm System and Management on GHG Emissions

Considered independently, six variables had a significant effect on emission intensity per kg of LW
sold (Table 3). Emissions were significantly lower under good than under poor livestock care management
controls, if technical advice was sought, if rotational grazing was used, and in CCBG rather than in CC
systems. Land and animal productivity affected the emissions, with lower emission intensities under
higher land and animal productivity. Furthermore, emission intensity was negatively correlated with
land and animal productivities (r = −0.46, p < 0.05; r = −0.87, p < 0.001, respectively). Weaning rate and
emission intensity were negatively correlated (r = −0.39, p < 0.05); however, a Mann-Whitney test did not
indicate a significant effect of weaning rate on emission intensity (p < 0.10, Table 3).
The set of variables that, considered independently, had a significant effect on emissions per
hectare of farmland differed from those that affected emission intensity per kg of LW sold, with the
exception of land productivity, which significantly affected both types of emissions, but in opposite
directions (Table 3). Emissions per hectare were significantly lower if little or no land had been
dedicated to improved pastures or annual forage crops, if mortality rate was low, if stocking rate was
low, and if the number of grazing paddocks per total land was low. Emissions were higher under
moderate than under low land productivity. Furthermore, land productivity and emissions per hectare
were positively correlated (r = 0.66, p < 0.001).
Eleven models for emissions per kg of LW sold and eight models for emissions per hectare
of farmland had significant (p < 0.05) values for the intercept and explanatory variables (Table 4).
All of the variables that individually had a significant effect on emission intensity (Table 3) yielded
significant models.
In the best model for explaining emissions per kg LW sold (Model 1, lowest AICc and highest D2 ),
animal and land productivities were significant explanatory variables (Table 4 and Figure 1). Systems
that had higher animal and higher land productivity emitted less than those systems with a lower
productivity. The calculated square deviance (D2 ) indicated that the model explained 51.2% of the
variation in the response variable. Models 2–3 performed worse in terms of AICc and D2 but were
plausible in terms of ΔAICc (ΔAICc < 7) and should rarely be dismissed [49]. Models 2–3 included
management care controls of livestock as an explanatory variable: systems that had good management
controls emitted less than those that did not. Models 4–9 performed worse than 1–3 but were not
necessarily dismissed (ΔAICc < 11) [49], and they included the type of production system, grazing
system and technical advice as significant explanatory variables: CCBG systems emitted less than
CC systems, rotational emitted less than did continuous grazing, and systems that received technical
advice emitted less than did those that did not. Models 10–11 had relatively little empirical support

125
Sustainability 2018, 10, 4228

(ΔAICc > 11) [49] and were dismissed. Within each model, the partial regression coefficients and
the ‘D2 change on deletion’ (%DCD, results not shown) indicated that animal productivity (Model
1), livestock care management (Model 3), type of production system (Model 4), and grazing system
(Model 5) had more weight in influencing emission intensity than land productivity.

Table 3. Individual effects of farm characteristics and management on greenhouse gas

emission intensity.

Farm Greenhouse Gases Emissions Intensity

Variable Level/Type kg CO2 e/kg LW Sold kg CO2 e/ha
Mean ± s.d. n Sig.a Mean ± s.d. n Sig.a
Land use
Land area used for improved pastures or 0/very low 21.29 ± 7.76 24 221 ± 199 24
n.s. **
annual forage crops (%) Low/moderate 18.28 ± 9.72 3 503 ± 184 3
No 22.28 ± 9.19 14 232 ± 263 14
Feed purchase n.s. n.s.
Yes 19.54 ± 6.12 13 273 ± 153 13
Beef cattle
Low 21.94 ± 7.39 14 257 ± 251 14
Average live weight of livestock (kg) n.s. n.s.
Moderate 19.91 ± 8.47 13 246 ± 175 13
Low 19.82 ± 6.25 14 237 ± 171 14
Cows to total animals rate (%) n.s. n.s.
Moderate 22.18 ± 9.37 13 268 ± 258 13
Low 22.00 ± 6.94 14 258 ± 258 14
Average weight of sold calf (kg) n.s. n.s.
Moderate 19.84 ± 8.85 13 246 ± 164 13
Low 21.31 ± 8.70 14 170 ± 75 14
Mortality rate (%) n.s. *
Moderate 20.58 ± 7.13 13 341 ± 277 13
Low 20.83 ± 9.65 14 145 ± 73 14
Stocking rate (LU/ha) n.s. ***
Moderate 21.10 ± 5.67 13 367 ± 256 13
Grazing infrastructures
Low 20.30 ± 8.21 14 196 ± 114 14
Water reservoirs/ha−1 (×10−3 ) n.s. n.s.
Moderate 21.67 ± 7.68 13 312 ± 268 13
Low 20.09 ± 8.56 14 157 ± 71 14
Grazing paddocks/ha (×10−3 ) n.s. *
Moderate 21.90 ± 7.21 13 354 ± 268 13
Technical management of the farm
Poor 24.23 ± 7.36 15 262 ± 245 15
Livestock care management controls * n.s.
Good 16.87 ± 6.59 12 239 ± 177 12
Reproductive management of the Year-round 23.72 ± 9.51 12 227 ± 269 12
n.s. n.s.
livestock (mating) Seasonal 18.75 ± 5.60 15 272 ± 165 15
No 23.96 ± 7.40 15 254 ± 245 15
Technical advice * n.s.
Yes 17.21 ± 6.92 12 249 ± 177 12
Continuous 27.65 ± 7.74 7 323 ± 350 7
Grazing system ** n.s.
Rotational 18.62 ± 6.55 20 227 ± 146 20
CC 23.60 ± 7.29 18 243 ± 225 18
Type of production system * n.s.
CCBG 15.68 ± 6.31 9 269 ± 200 9
Reproductive efficiency
Low 23.67 ± 7.53 14 262 ± 252 14
Weaning rate (%) (*) n.s.
Moderate 18.04 ± 7.34 13 241 ± 173 13
System productivity
Low 24.28 ± 7.78 14 148 ± 67 14
Land productivity (kg LW sold/ha) * ***
Moderate 17.38 ± 6.40 13 364 ± 261 13
Low 26.00 ± 6.27 14 262 ± 253 14
Animal productivity (kg LW sold/LU) *** n.s.
Moderate 15.53 ± 5.39 13 241 ± 172 13
LU, Livestock Units. LW, Live Weight. CC, Cow-calf. CCBG, Cow-calf + Backgrounding. a Sig. = significance based
on Mann-Whitney test. (*) = p < 0.10, * = p < 0.05, ** = p < 0.01, *** = p < 0.001.

126
 Table 4. Generalized linear models (GLM) for the response in emission intensity (kg CO2 e/kg LW sold, and as kg CO2 e/ha) of beef cattle farms to farm management
and characteristics.

Livestock Technical Grazing Production Animal Land Mortality Stocking Grazing

Emission Model Land Use Sig. AICc ΔAICc D2 (%)
Care Advice System System Productivity Productivity Rate Rate Paddocks
1 +0.459 *** +0.218 * *** 176.67 0.0 51.23
2 +0.515 *** *** 177.78 1.1 43.81
3 +0.360 ** +0.332 ** ** 182.43 5.8 39.83
4 +0.342 ** +0.261 ** ** 184.88 8.2 34.22
Sustainability 2018, 10, 4228

kgCO2 e 5 +0.330 ** +0.264 * ** 185.23 8.6 33.39

kg−1 6 +0.282 * +0.287 ** ** 186.07 9.4 31.34
LW sold 7 +0.409 ** ** 186.29 9.6 23.45
8 +0.396 ** ** 186.69 10.0 22.34
9 +0.362 ** * 187.00 10.3 21.44
10 +0.334 ** * 187.94 11.3 18.74
11 +0.331* * 188.20 11.5 17.97
1’ −0.784 *** −0.675 *** *** 334.64 0.0 57.39
2’ −0.748 *** −0.442 * *** 341.82 8.2 45.25
3’ −0.929 *** *** 342.02 8.4 39.32
kg CO2 e 4’ −0.903 *** *** 342.98 9.3 37.29
ha−1 5’ −0.811 *** ** 346.01 12.4 30.45
6’ −0.699 ** −0.620 * ** 346.83 13.2 34.93
7’ −0.698 ** * 349.08 15.4 22.81
8’ −0.823 ** * 351.084 17.4 17.45

127
Partial regression ß coefficients, with their statistical significance when the variable is ‘0’, statistical significance of the model (Sig.) based on an omnibus test, Akaike’s information
criteria (AICc), ΔAICc and square deviance (D2 ) are given. If β is > 0, emissions and the variable are positively correlated and if β is < 0, emissions and the variable are negatively
correlated. Only statistically significant variables (based on Wald’s chi-square test) are shown. Empty cells indicate variables not included in a given model. * = p < 0.05, ** = p < 0.01, ***
= p < 0.001. ΔAICc calculated as: ΔAICc = AICci − AICcmin , for i = 1, 2, . . . , R, where AICcmin denotes the minimum of the AICc values for the R models. D2 calculated as: D2 = (D0 −
Dmodel )/D0 , where D0 is the deviance of the null model (with intercept, only), and Dmodel is the deviance of the analyzed model.
 NJ&2HNJ/:VROG NJ&2HKD

02'(/ 02'(/¶
$QLPDOSURGXFWLYLW\S /DQGSURGXFWLYLW\S  /DQGSURGXFWLYLW\S *UD]LQJSDGGRFNVWRWDOODQGS 
 
 
 
   
   
Sustainability 2018, 10, 4228

 

NJ&2HKD
NJ&2HKD
 
 

NJ&2HNJ/:VROG
NJ&2HNJ/:VROG
   
ORZ PRGHUDWH ORZ PRGHUDWH ORZ PRGHUDWH ORZ PRGHUDWH

02'(/ 02'(/¶
$QLPDOSURGXFWLYLW\S /DQGSURGXFWLYLW\S  0RUWDOLW\UDWHS 
ϯϬ
 ϰϬϬ
Ϯϱ
ϮϬ  ϯϬϬ
ϭϱ  ϮϬϬ
ϭϬ

NJ&2HKD
NJ&2HKD

 ϭϬϬ

128
ϱ

ŬŐKϮĞͬŬŐ>tƐŽůĚ
Ϭ  Ϭ
ORZ PRGHUDWH ORZ PRGHUDWH ORZ PRGHUDWH

02'(/ 02'(/¶
/LYHVWRFNFDUHFRQWUROVS  /DQGSURGXFWLYLW\S  6WRFNLQJUDWHS 
 ϯϬ

 Ϯϱ
 ϮϬ 
 ϭϱ 
 ϭϬ
NJ&2HKD


 ϱ

ŬŐKϮĞͬŬŐ>tƐŽůĚ
 Ϭ 

ŬŐKϮĞŬŐͲϭ ƚŽƚĂů>tƐŽůĚ
SRRU JRRG ůŽǁ ŵŽĚĞƌĂƚĞ ORZ PRGHUDWH


Figure 1. Marginal means and standard error of the most significant GLM models for the response in emission intensity (kg CO2 e/kg LW sold, and kg CO2 e/ha) of
beef cattle farms in San Luis province, central Argentina. Differences were tested using Wald’s chi-square test.
Sustainability 2018, 10, 4228

In the best model for explaining emissions per hectare of farmland (Model 1’, lowest AICc and
highest D2 ), land productivity and the number of grazing paddocks per total land were significant
explanatory variables (Table 4 and Figure 1). Systems that had lower land productivity emitted less
than did those systems with a higher land productivity. In addition, systems that had less grazing
paddocks emitted less. In this model, the partial regression coefficients indicated that land productivity
had more weight than the number of grazing paddocks. Calculated square deviance (D2 ) indicated
that the model explained 57.4% of the variation in the response variable. Models 2’-4’ performed worse
than model 1’ in terms of AICc and D2 but were not necessarily dismissed (ΔAICc < 11) [49], and they
included the mortality rate and stocking rate as significant explanatory variables: systems that had a
lower mortality rate emitted less than did those that had a higher mortality rate, and systems that had
a lower stocking rate emitted less than did those that had a higher stocking rate. Models 5’–8’ had
relatively little empirical support (ΔAICc > 11) [49] and were dismissed. Within each model, the partial
regression coefficients and the ‘D2 change on deletion’ (%DCD, results not shown) indicated that the
number of grazing paddocks (Model 1’) and mortality rate (Model 2’) had less weight in influencing
emissions than land productivity.

3.3. Farm Typification

The PCA identified the following five groups of farms (Tables 5–7):

• Group I (23% of farms): ‘High emitters per LW sold’ (higher emitters than group V) and ‘low
emitters per hectare’ (lower emitters than group II). ‘Worse management’ and ‘low stocking
rates’ (lower stocking rates than group II). Only cow-calf systems. Highest proportion of farms
with continuous grazing. On those farms, all of the land area consists of natural grasslands,
and off-farm feeds are not used. Lowest percentage of farms that have three or more types
of livestock care management controls. Highest percentage of farms with year-round mating.
Highest proportion of farms without any technical advice. Low weaning rates (lower weaning
rates than group IV). ‘Low land and animal productivities’ (lower land productivity than groups
II and V, and lower animal productivity than group V).
• Group II (30% of farms): ‘Intermediate emitters per LW sold’ and ‘high emitters per hectare’
(higher emitters per hectare than group I). ‘Medium level of management’ and ‘high stocking
rates’ (higher stocking rates than group I). Cow-calf systems and rotational grazing predominate.
Almost all of the land area consists of natural grasslands, and most of the farms use off-farm
feeds (higher percentage than group I and III). Most of the farms have three or more livestock
management controls, 50% of farms have year-round mating, and 78% of farms receive no
technical advice (less technical advice than groups III and IV). Intermediate weaning rates. ‘High
land productivity’ (higher than group I) and ‘intermediate animal productivity’.
• Group III (17% of farms): ‘Intermediate emitters per LW sold and per hectare’. ‘Suitable farm
management’ and ‘intermediate stocking rates’. Cow-calf or mixed CCBG systems, and all the
farms use rotational grazing. The entire land area consists of natural grasslands, and off-farm
feeds are not used. All of the farms implemented at least 3 types of livestock management
controls, 80% of the farms had seasonal mating of the herd, and all farms have technical advice.
Intermediate weaning rates. ‘Intermediate land and animal productivity’.
• Group IV (20% of farms): ‘Intermediate emitters per LW sold and per hectare’. ‘Suitable farm
management’, and ‘intermediate stocking rates’. Cow-calf, BG or mixed CCBG systems, and
all the farms have rotational grazing. Almost all of the land area consists of natural grasslands,
and most farms use off-farm feeds. All of the farms implement at least 3 types of livestock
management controls and have seasonal mating of the herd, and 83% of farms have technical
advice. High weaning rates (higher weaning rates than group I). ‘Intermediate land and
animal productivities’.

129
Sustainability 2018, 10, 4228

• Group V (10% of the farms): ‘Low emitters per LW sold’ (lower emitters than group I), and
‘intermediate emitters per hectare’. ‘Good farm management’ and ‘intermediate stocking rates’.
None of the farms were exclusively cow-calf systems. All of the farms had rotational grazing.
Relatively high proportion of land used for introduced pastures and annual forage crops, and
67% of farms used off-farm feeds (higher percentage of farms than in groups I and III). All of the
farms implemented at least 3 types of livestock management controls, had seasonal mating of the
herd, and 67% of farms had technical advice. Intermediate weaning rates. ‘High land and animal
productivities’ (higher than group I).

Table 5. Mean values for continuous variables by cluster group.

Cluster Group
Variable I II III IV V Sig.a
n=7 n=9 n=5 n=6 n=3
Socio-economic data
Age (years) 61 58 48 49 55 n.s.
+ Hired labor (WU/LU) (×10−3 ) 1.0 a 0.2 a 4.6 b 2.9 ab 1.3 ab ***
Land use
+ 1077 a 1673 a
Total land area (ha) 7010 b 3284 ab 10,200 ab **
+ Land area used for native pastures (%) 64 a
100 b 98 b 100 b 94 ab **
+ 26 a
Land area used for improved pastures (%) 0b 0b 0b 6 ab ***
Land area used for forage crops (%) 0b 2 ab 0b 0b 10 a *
Beef cattle
+ 51.6 a
Total livestock units 194.4 ab 482.1 b 328.0 ab 1207.0 b ***
Mortality rate (%) 11.9 10.0 2.3 2.2 2.2 n.s.
Stocking rate (LU/ha) 0.07 a 0.19 b 0.08 ab 0.10 ab 0.19 ab *
Grazing infrastructures
Water reservoirs per ha (×10−3 ) 3.0 ab 5.2 a 0.9 b 1.4 ab 1.4 ab *
Water reservoirs/LU (×10−3 ) 46 b 27 ab 12 a 17 ab 8a **
+ Grazing paddocks/ha (×10−3 ) 2.6 7.2 1.1 2.4 2.2 n.s.
System productivity
Average live weight of livestock (kg) 272 284 302 283 271 n.s.
Weaning rate (%) 49 a 63 ab 69 ab 82 b 73 ab *
+ Land productivity (kg LW sold/ha) 4.7 a 20.3 b 11.3 ab 19.6 ab 52.9 b ***
Animal productivity (kg LW sold/LU) 74 a 123 ab 160 ab 144 ab 283 b *
Farm greenhouse gases emission intensity
kg CO2 e/kg LW sold 27 b 20 ab 15 ab 19 ab 8a *
kg CO2 e/ha 121 a 372 b 166 ab 266 ab 403 ab **
+ Variables used in the principal component analysis and in the cluster analysis. a Sig. = significance based on the
Kruskal–Wallis test. * = p < 0.05, ** = p < 0.01, *** = p < 0.001. Different letters in the same row indicate significant
differences between groups (Dunn–Bonferroni post-hoc test).

Table 6. Frequency (% of farms) of discrete variables by cluster group.

Cluster Group
Variable I II III IV V Sig.a
n=7 n=9 n=5 n=6 n=3
Socio-economic data
+Level of education of farmer 1
None 0 22 20 0 0 n.s.
Primary or secondary school 100 b 78 b 20 a 0a 100 b ***
Higher education 0a 0a 60 b 83 b 0a ***

130
Sustainability 2018, 10, 4228

Table 6. Cont.

Cluster Group
Variable I II III IV V Sig.a
n=7 n=9 n=5 n=6 n=3
Type of production system
Cow-calf 100 b 78 b 60 ab 50 a 0a *
Backgrounding 0 11 0 17 33 n.s.
Cow-calf + backgrounding 0 11 40 33 67 n.s.
Grazing system
Continuous 71 b 22 a 0a 0a 0a **
Rotational 22 a 78 ab 100 b 100 b 100 b **
+ Feed purchase
Yes 0a 89 b 0a 83 b 67 b **
No 100 b 11 a 100 b 17 a 33 a *
Technical management of the farm
+ Livestock care controls 2,3
None 43 13 0 0 0 n.s.
One or two control types 43 25 0 0 0 n.s.
Three or more control types 14 a 62 b 100 b 100 b 100 b ***
Reproductive management of the livestock 3
Year-round mating 100 b 50 a 20 a 0a 0a **
Seasonal mating 0a 50 b 80 b 100 b 100 b **
+ Technical advice

None 100 c 78 b 0a 17 a 33 ab **
Veterinarian and/or agronomist 0a 22 ab 100 c 83 c 67 bc **
+ Variables used in the principal component analysis and in the cluster analysis. 1 Remaining farmers, Do not
know/No answer. 2 Types of livestock care controls: body condition, teeth examination, rectal palpation/ecography,
parasite control, reproductive vaccine, bull review control. 3 n = 27 (backgrounding farms excluded). a Sig. =
significance based on Pearson’s chi-squared test. * = p < 0.05, ** = p < 0.01, *** = p < 0.001. Different letters in the
same row indicate significant differences between groups.

Table 7. Main characteristics of each cluster group: socio-economic data, land use, beef cattle, feed
purchase, technical management of the farm, system productivity, greenhouse gases emission, grazing
system and type of production system. Based on Tables 5 and 6.

Cluster Group
I II III IV V
Main education level PS PS HE HE PS
Hired labor a a b ab ab
Total land area a a b ab ab
Land area used for native pastures b b b ab a
Land area used for improved pastures a a a ab b
Land area used for annual forage crops a ab a a b
Total livestock units a ab b ab b
Stocking rate a b ab ab ab
Dependence on off-farm feeds a b a b b
Livestock care controls: ≥3 control types a b b b b
Technical advice: Veterinarian and/or
a ab c c bc
Agronomist
Weaning rate a ab ab b ab
Land productivity a b ab ab b
Animal productivity a ab ab ab b
Emission intensity per LW sold b ab ab ab a
Emission intensity per hectare a b ab ab ab
Main grazing system CON ROT ORO ORO ORO
Main system OCC CC CC CC CCBG
Main reproductive management OYR YRS S S S
PS = Primary or secondary school. HE = Higher education. CON = Continuous, ROT = Rotational, ORO = Only
rotational, OCC = Only cow-calf, CC = Cow-calf, CCBG = Cow-calf and backgrounding, OYR = Only year-round,
YR = Year-round, YRS = Year-round/seasonal, S = Seasonal. Different letters in the same row indicate significant
differences between groups (based on Tables 5 and 6).

131
Sustainability 2018, 10, 4228

4. Discussion
GHG farm emissions varied widely among the 30 farms surveyed in the semiarid rangelands
of central Argentina, which reflected the high diversity in the types of production systems [26,56].
Variability is especially high in studies that have been based on actual farm survey data [14,26].
In our study, on a product sold basis, cow-calf systems emitted more GHG than backgrounding
systems. Similar results have been reported in grassland-based beef systems in Uruguay [14,15,57]
and Argentina [58]. In our study, the GHG emissions of cow-calf systems were similar to those of 295
cow-calf farms in Canada [26] and the cow-calf systems based on native and improved grasslands in
Uruguay [14]. Emissions from backgrounding systems were similar to those from background-finishing
systems that had seeded pastures and feedlots in Uruguay [57].
On a farm-area basis, in our study, GHG emissions did not differ significantly among types of
systems. The average was much lower than previously reported values, which ranged between 265 and
9782 [26], and between 2334 and 3037 [59] in Canadian beef cattle production systems, between 1490
and 2827 in Uruguayan beef systems [14], and between 7902 and 10,913 in New Zealand pasture-based
dairy systems [60]. The higher stocking rates in those studies (0.31, 0.77 and 2.3–3.0 LU/ha in Canadian,
Uruguayan and New Zealand systems, respectively, versus 0.13 LU/ha in our study) were mainly
responsible for the differences in emissions between those studies and ours. In our study, the emissions
per hectare and stocking rate were positively correlated (r = 0.900, p < 0.001). In beef systems in the
Brazilian Amazon [61] and in dairy systems in Ireland [62], emissions per hectare and stocking rates
were positively correlated. Livestock density on extensively managed grazing lands are relatively
low; therefore, CH4 emissions per unit area from these grazing lands is much lower than those from
intensively managed grazing lands [33,63]. The contribution of extensively managed grasslands to
GHG emissions is expected to be low per unit area because of low livestock densities and agronomic
inputs, although the absolute global contribution might be high because of their large land area [63].
In our study, on a product sold basis, animal productivity was the variable that best explained
the largest amount of variance in emission intensity, which was negatively correlated with
productivity. To a lesser degree, land productivity and emission intensity were negatively correlated.
Improving production efficiency has been recommended as a strategy to mitigate GHG emissions
in beef systems [14,15,26,57,64–66]. For instance, Alemu et al. [26] found that low-emitting farms
had higher animal and land productivities than high-emitting farms in Canadian cow-calf systems.
In French suckler-beef production farms, animal productivity was the main factor influencing GHG
emissions [64], which suggested that technical efficiency was a factor. Becoña et al. [14] found that
beef farm productivity was one of the main determinants of GHG emissions in Uruguayan cow-calf
systems. The same negative correlation was found in dairy systems [67,68], mainly because emissions
are spread over more units of output per cow, which dilutes emission intensity. Productivity gains
are generally achieved through improved husbandry practices and technologies that increase the
proportion of resources used for production purposes rather than for the maintenance of the animals,
which contribute to emission reductions [1]. Improved farm productivity can result from a combination
of several types of strategies.
On the beef farms in our study, continuous stocking practices emitted significantly more GHG per
product sold than rotational stocking. Beef cattle in rotational stocking systems emitted less methane
than cattle in continuous grazing [35]. Furthermore, good grazing management can have a positive
impact on soil carbon sequestration [1].
Improved livestock care management was associated with reduced GHG emission intensity per
kg LW sold in our study. Improved animal health can increase herd productivity and reduce GHG
emission intensity [24]. Along with improved reproduction management, improved animal health
helps to reduce the unproductive portion of the herd and associated emissions, and concomitantly,
these measures increase productivity [1]. Preventive health measures can play a role in increasing
growth and fertility rates, which improve animal and herd performance [1]. Llonch et al. [27] reported
a reduction in rumen methanogenesis in response to an increase in production efficiency caused

132
Sustainability 2018, 10, 4228

by improvements in the health status of the herd, which is a win-win strategy, because it increases
environmental sustainability and animal welfare.
In our study, farms that had received technical advice had lower emissions per unit of product
sold, which reflected the importance of technical advice in grazing management planning, feeding,
health care, the reproductive management of the herd, and overall farm system management [69,70].
Land-related variables can affect GHG emissions from animals through diet quality [26].
Diet digestibility directly reduces CH4 emission intensity [64,71], which was apparent on farms
that had an increased area of improved pastures, including seeded pastures, oversowing with legumes,
and annual winter crops for grazing [14]. In our study, such an effect was not apparent, probably
because of the small proportion of the farmland that had been used for improved pastures or annual
forage crops (mean = 6%, vs. 20.5% in the study by Becoña et al. [14]).
Many of those husbandry practices are associated with increases in productivity, which suggests
that an economic benefit can be realized with a concurrent reduction in GHG emissions [27].
Strategies that both improve production efficiency and reduce GHG emissions are those most attractive
to and most likely to be adopted by farmers [26]. Further studies should compare the economic impact
of several measures to mitigate GHG emissions and willingness to adopt them in our study area.
In our study, emission intensity per hectare of farmland was positively correlated with stocking
rate and land productivity. Similar results were reported by Becoña et al. [14] in beef cow-calf systems.
In Irish dairy farms, Casey and Holden [16] found a significant positive correlation between stocking
rate and the amount of GHG emissions per hectare. Bava et al. [68] found a strong positive correlation
between emissions per land area and stocking rate in dairy systems. Stocking rate and total dry
matter intake are the main factors driving production per hectare and GHG emissions from grazed
pastoral systems [7]. The number of grazing paddocks per hectare and the proportion of land used
for improved pastures and annual forage crops were positively correlated with GHG emissions per
hectare of land area in our study. Higher stocking rates and land productivity, coupled with higher
density of grazing paddocks and land use for improved pastures and forage crops, reflect a certain
degree of intensification of the farming system, i.e., intensification implied higher emissions per hectare.
Bava et al. [68] concluded that intensification, defined as the increase in output per hectare, invariably
led to higher emissions on a per-area basis. Nevertheless, the emissions per unit of product and
land productivity were negatively correlated, which illustrates the potential trade-off between carbon
efficiencies per unit of product and per unit of land, i.e., is it possible to reduce emissions per unit of
land and per unit of product at the same time?
The CA indicated that, if GHG emissions are evaluated on a land-unit basis, farms of group 1
had low emissions and were very extensive in terms of land use. They had low stocking rates, a low
dependence on off-farm feeds, land productivity, and low proportion of land used for improved
pastures or annual crops. Farms in that group, however, had the lowest level of husbandry practices in
terms of livestock care controls and reproductive management, technical advice, and grazing system,
low weaning rate and animal productivity, and concomitantly, they had high emissions per product
sold. From that ‘base-line’ traditional farming system, strategies can differ considerably in practice
and results, in terms of farm productivity and emissions. Farms in group II intensified the system by
increasing the stocking rates and dependence on off-farm feeds, and they improved some husbandry
practices, maintained emissions per product sold, but increased emissions per hectare. Farms in group
V had a higher proportion of land as improved pastures and annual forage crops, medium stocking
rates, improved livestock husbandry practices, and had intermediate levels of emissions per hectare.
This group had lower emissions per product sold than group I because of those improvements, but
also because of the high proportion of backgrounding on the farms in this group. Nevertheless, it has
to be taken into account that only three farms belonged to group V. Groups III and IV had higher levels
of husbandry practices than groups I and II, but they did not have stocking rates that were as high as
those in group II. Thus, those groups (III and IV) had intermediate levels of farm productivity and
emissions per product sold and per hectare.

133
Sustainability 2018, 10, 4228

The CA suggested that farms that had a high level of husbandry ‘intensification’ through livestock
care and reproductive management achieved high animal productivity and, therefore, low GHG
emissions per product sold compared to ‘base-line farms’ (group I). Thus, if land productivity
is increased by using that high-output animal strategy, emissions per hectare can be limited to
intermediate levels. However, if land productivity is maximized through high stocking rates, emissions
per hectare is the highest, as in the case of group II. Becoña et al. [14] stated that both emissions per
unit of land and per unit of product can be reduced concurrently and suggested that the key factor
is reducing stocking rate (or increasing forage allowance) in grazing beef cow-calf systems. GHG
emission intensity can be reduced through changes in animal husbandry practices that increase animal
outputs [14,64]. Casey and Holden [16] suggested that it is physically and biologically possible to
achieve low emissions, both per unit of land and per product, by using high-output cows at low
stocking rates in dairy systems. A move toward fewer cows producing more milk at lower stocking
rates is required, representing an extensification in terms of area, but an intensification in terms of
animal husbandry practices. In a simulation experiment on pasture-based dairy farms in New Zealand,
Beukes et al. [60] maintained production but reduced GHG emissions per unit of land and per unit
of product by increasing efficiency (e.g., reducing the number of non-productive animals in the herd,
among other mitigation strategies), which allowed stocking rates to be reduced. The mitigation of
GHG emissions per unit of product should be based on the intensification of husbandry systems rather
than on land intensification, which might lead to potential losses in ecosystem service provisioning,
increases in GHG emissions per unit of area and other environmental impacts, such as eutrophication
and acidification [15].
Among the beef cattle farms in our study, those in groups III and IV could further reduce
emission intensity by adopting practices, such as improving feed quality [22,26,64], using superior
animal genetics [72], or increasing the proportion of backgrounding vs. cow-calf in the farm system.
Feed quality can be increased by applying seeding grasses to improve native pastures, annual forage
cropping, and by purchasing high-quality off-farm feeds. However, introduced grasses can increase the
impact on native grasslands, with potential biodiversity, wildlife habitat and landscape losses [15,57].
The mitigation of climate change should not be associated with directly reducing biodiversity [15].
In several regions of the world, pasture intensification has been used to increase productivity, incomes,
and mitigate GHG, but has increased rangeland degradation [32]. Annual cropping systems have
relatively high levels of agronomic inputs and nutrient leakage, frequent and significant disturbances
of the soil surface, and net losses of soil organic content [33]. In addition, CO2 emissions derived
from fertilizers and machinery operations for annual forage crops are high [26]. Feed quality can
be improved by purchasing high-quality feeds, but the embedded emissions associated with feed
production should not be ignored. Alemu et al. [26] found that minimizing purchased cereal grain
and forage per unit cow reduced the emissions associated with the production and transportation
of farm inputs. In strategies, such as improving genetic merit, the animals have to be selected
not only for their high efficiency in transforming feeds, but also for their ability to adapt to rough
environments and low-quality feeds [73], which are characteristic of the semi-arid rangelands of central
Argentina. In addition, to reduce emissions per unit of product, farmers can increase the proportion
of backgrounding versus cow-calf in their system. However, this strategy can transfer the negative
environmental impacts of the cow-calf phase to other areas, i.e., the emissions of the replacement stock,
if purchased, have occurred elsewhere on other farms [74].
Our results from actual semi-arid rangeland beef systems in central Argentina suggest that the
implementation of relatively easy-to-adopt farming management practices has considerable potential
for reducing GHG emissions per unit of product and per unit of land area. At the same time, the
preservation of rangeland ecosystem services should be a target.
The expansion of agriculture and an increase in the intensification of livestock systems have
challenged the integrity of rangelands in Argentina and worldwide. Future research should assess the
ecosystem services provided by the beef production systems in the semi-arid rangelands of Argentina,

134
Sustainability 2018, 10, 4228

e.g., wildlife biodiversity and landscape preservation, animal welfare, nutrient cycling, hydrologic
conditions, control of invasive plant species, and carbon sequestration. Grazing lands have a high
potential for carbon sequestration [23,75,76], which can, at least partially, mitigate the GHG emissions
from ruminant production systems [77]. Extensive livestock grazing systems had a lower GHG
emission intensity if soil carbon uptake had been included in the emission inventory [15,65,78–81],
particularly for low-input or small-scale grazing systems [20,81]. Therefore, land-use decisions
should be informed by all environmental factors, negative impacts—not only GHG emissions—and
ecosystem services. In order to increase the sustainability and efficiency of beef livestock systems in
the Argentinean semi-arid rangelands, future studies should use an integrated, holistic approach.

5. Conclusions
This study assessed the relationships between GHG emissions and characteristics and the
management practices of commercial farms in extensive beef systems that are based on the natural
rangelands in the semi-arid Central Region of Argentina. The results suggest that the implementation
of realistic, relatively easy-to-adopt farming management practices has a considerable potential to
mitigate GHG emissions. Emissions per product sold were low on farms that had improved livestock
care management, had rotational grazing, received technical advice, and had high animal and land
productivities. The emissions per hectare of farmland were low on farms that had low stocking rates, a
low number of grazing paddocks, little or no land dedicated to improved pastures and annual forage
crops, and low land productivity.
Therefore, in our study, the set of variables that influenced the emissions per hectare of farmland
differed from those that affected the emissions per unit of product, and land productivity affected
the two types of emission expressions in opposite directions, which suggests a potential trade-off
between the mitigation of GHG emissions per unit of product and per unit of land. Given that GHG
emissions per product and per hectare of farmland differ in their implications for the assessment of the
environmental impacts of food production (e.g., global vs. local scales, intensification processes), both
measures should be taken into account and reconciled as much as possible.
To identify ways to increase the sustainability and efficiency of the management of beef livestock
systems in the Argentinean semi-arid rangelands, future studies should use an integrated, holistic
approach in which all negative environmental impacts and ecosystem service provisioning, e.g.,
diversity preservation and carbon sequestration, should be assessed.

Author Contributions: Conceptualization, M.I.N., O.B., L.P. and R.R.; Data curation, M.I.N.; Formal analysis,
M.I.N., O.B. and R.R.; Funding acquisition, M.I.N.; Investigation, M.I.N. and L.P.; Methodology, M.I.N., O.B. and
R.R.; Resources, M.I.N. and L.P.; Supervision, O.B. and R.R.; Validation, O.B. and R.R.; Writing—original draft,
O.B. and M.I.N.; Writing—review and editing, O.B., R.R. and M.I.N.
Funding: This research was funded by the Instituto Nacional de Tecnología Agropecuaria (INTA), Argentina.
Acknowledgments: The authors are grateful to C.A. Frasinelli for his contribution and technical advice, and to
the farmers that participated in the study.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to
publish the results.

Appendix A
The IPCC (2006) [42] equations used in the calculations of the on-farm CH4 and N2 O gases
emissions were: 10.3, 10.4, 10.6, 10.8, 10.13, 10.14, 10.15, 10.16, 10.17, 10.18, 10.19, 10.20, 10.21, 10.31,
10.32, 10.33, 11.1, 11.5, and 11.11.

135
Sustainability 2018, 10, 4228

References
1. Gerber, P.J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling
Climate Change through Livestock e a Global Assessment of Emissions and Mitigation Opportunities; Food and
Agriculture Organization of the United Nations (FAO): Rome, Italy, 2013; ISBN 978-92-5-107921-8.
2. United Nations Department of Economic and Social Affairs. Available online: http://www.un.org/en/
development/desa/news/population/un-report-world-population-projected-to-reach-9-6-billion-by-
2050.html (accessed on 26 September 2018).
3. Delgado, C.L. Rising demand for meat and milk in developing countries/implications for grasslands-based
livestock production. In Grassland: A Global Resource; McGilloway, D.A., Ed.; Wageningen Academic
Publishers: Wageningen, The Netherlands, 2005; pp. 29–40, ISBN 978-90-76998-71-8.
4. Garnett, T. Livestock-related greenhouse gas emissions: Impacts and options for policy makers. Environ. Sci.
Policy 2009, 12, 491–503. [CrossRef]
5. Rojas-Downing, M.M.; Nejadhashemi, A.P.; Harrigan, T.; Woznicki, S.A. Climate change and livestock:
Impacts, adaptation, and mitigation. Clim. Risk Manag. 2017, 16, 145–163. [CrossRef]
6. Opio, C.; Gerber, P.; Mottet, A.; Falcucci, A.; Tempio, G.; Macleod, M.; Vellinga, T.; Henderson, B.; Steinfeld, H.
Greenhouse Gas Emissions from Ruminant Supply Chains—A Global Life Cycle Assessment; Food and Agriculture
Organization of the United Nations (FAO): Rome, Italy, 2013; p. 191, ISBN 978-92-5-107945-4.
7. De Klein, C.A.M.; Pinares-Patiño, C.; Waghorn, G.C. Greenhouse gas emissions. In Environmental Impacts of
Pasture-Based Farming; McDowell, R.W., Ed.; CABI: Wallingford, UK, 2008; pp. 1–32, ISBN 978-18-4-593411-8.
8. Ministerio de Economía y Finanzas Públicas. Complejo Ganadero Vacuno. Serie “Complejos Productivos”.
Secretaría de Política Económica y Planificación del Desarrollo. Gobierno Argentino. Available
online: https://www.economia.gob.ar/peconomica/docs/Complejo_Ganadero_vacuno.pdf (accessed on
26 September 2018).
9. Miazzo, D.; Pisani Claro, N. Carnes Argentinas. Actualidad, Propuestas y Futuro; Fundación Agropecuaria para
el desarrollo de Argentina (FADA), Sitio Argentino de Producción Animal: Río Cuarto, Cordoba, Argentina,
2015; pp. 1–37. Available online: http://www.produccion-animal.com.ar/informacion_tecnica/origenes_
evolucion_y_estadisticas_de_la_ganaderia/00-origenes_evolucion_y_estadisticas_de_la_ganaderia.htm
(accessed on 28 September 2018).
10. Rearte, D.H.; Pordomingo, A.J. The relevance of methane emissions from beef production and the challenges
of the Argentinean beef production platform. Meat Sci. 2014, 98, 355–360. [CrossRef] [PubMed]
11. Segundo Informe Bienal de Actualización de la República Argentina a la Convención Marco de las
Naciones Unidas sobre el Cambio Climático. Ministerio de Ambiente y Desarrollo Sustentable. República
Argentina. 2017, pp. 37–69. Available online: http://euroclimaplus.org/intranet/_documentos/repositorio/
02%20Bienal%20Convenci%C3%B3n%20ONU%20cambio%20clim%C3%A1tico_2017.pdf (accessed on
28 September 2018).
12. Bárbaro, N.; Gere, J.; Gratton, R.; Rubio, R.; Williams, K. First measurements of methane emitted by grazing
cattle of the Argentinean beef system. N. Z. J. Agric. Res. 2008, 51, 209–219. [CrossRef]
13. Reisinger, A.; Ledgard, S. Impact of greenhouse gas metrics on the quantification of agricultural emissions
and farm-scale mitigation strategies: A New Zealand case study. Environ. Res. Lett. 2013, 8, 025019.
[CrossRef]
14. Becoña, G.; Astigarraga, L.; Picasso, V.D. Greenhouse gas emissions of beef cow–calf grazing systems in
Uruguay. Sustain. Agric. Res. 2014, 3, 89–105. [CrossRef]
15. Picasso, V.D.; Modernel, P.D.; Becoña, G.; Salvo, L.; Gutiérrez, L.; Astigarraga, L. Sustainability of meat
production beyond carbon footprint: A synthesis of case studies from grazing systems in Uruguay. Meat Sci.
2014, 98, 346–354. [CrossRef] [PubMed]
16. Casey, J.W.; Holden, N.M. The relationship between greenhouse gas emissions and the intensity of milk
production in Ireland. J. Environ. Qual. 2005, 34, 429–436. [CrossRef] [PubMed]
17. Ross, S.A.; Topp, C.F.E.; Ennos, R.A.; Chagunda, M.G.G. Relative emissions intensity of dairy production
systems: Employing different functional units in life-cycle assessment. Animal 2017, 11, 1381–1388. [CrossRef]
[PubMed]

136
Sustainability 2018, 10, 4228

18. Halberg, N.; van der Werf, H.M.G.; Basset-Mens, C.; Dalgaard, R.; de Boer, I.J.M. Environmental assessment
tools for the evaluation and improvement of European livestock production systems. Livest. Prod. Sci. 2005,
96, 33–50. [CrossRef]
19. Veysset, P.; Lherm, M.; Bébin, D. Energy consumption, greenhouse gas emissions and economic performance
assessments in French Charolais suckler cattle farms: Model-based analysis and forecasts. Agric. Syst. 2010,
103, 41–50. [CrossRef]
20. Cottle, D.J.; Nolan, J.V.; Wiedemann, S.G. Ruminant enteric methane mitigation: A review. Anim. Prod. Sci.
2011, 51, 491–514. [CrossRef]
21. Gerber, P.J.; Hristov, A.N.; Henderson, B.; Makkar, H.; Oh, J.; Lee, C.; Meinen, R.; Montes, F.; Ott, T.; Firkins, J.;
et al. Technical options for the mitigation of direct methane and nitrous oxide emissions from livestock:
A review. Animal 2013, 7, 220–234. [CrossRef] [PubMed]
22. Hristov, A.N.; Oh, J.; Lee, C.; Meinen, R.; Montes, F.; Ott, T.; Firkins, J.; Rotz, A.; Dell, C.; Adesogan, C.;
Yang, W.; et al. Mitigation of Greenhouse Gas Emissions in Livestock Production—A Review of Technical Options
for Non-CO2 Emissions; Food and Agriculture Organization of the United Nations (FAO): Rome, Italy, 2013;
pp. 1–206, ISBN 978-92-5-107659-0.
23. Hristov, A.N.; Oh, J.; Firkins, J.L.; Dijkstra, J.; Kebreab, E.; Waghorn, G.; Makkar, H.P.S.; Adesogan, A.T.;
Yang, W.; Lee, C.; et al. Special topics-Mitigation of methane and nitrous oxide emissions from animal
operations: I. A review of enteric methane mitigation options. J. Anim. Sci. 2013, 91, 5045–5069. [CrossRef]
[PubMed]
24. Hristov, A.N.; Ott, T.; Tricarico, J.; Rotz, A.; Waghorn, G.; Adesogan, A.; Dijkstra, J.; Montes, F.; Oh, J.;
Kebreab, E.; et al. Special topics-Mitigation of methane and nitrous oxide emissions from animal operations:
III. A review of animal management mitigation options. J. Anim. Sci. 2013, 91, 5095–5113. [CrossRef]
[PubMed]
25. Gerber, P.J.; Mottet, A.; Opio, C.I.; Falcucci, A.; Teillard, F. Environmental impacts of beef production: Review
of challenges and perspectives for durability. Meat Sci. 2015, 109, 2–12. [CrossRef] [PubMed]
26. Alemu, A.W.; Amiro, B.D.; Bittman, S.; MacDonald, D.; Ominski, K.H. Greenhouse gas emission of Canadian
cow-calf operations: A whole-farm assessment of 295 farms. Agric. Syst. 2017, 151, 73–83. [CrossRef]
27. Llonch, P.; Haskell, M.J.; Dewhurst, R.J.; Turner, S.P. Current available strategies to mitigate greenhouse
gas emissions in livestock systems: An animal welfare perspective. Animal 2017, 11, 274–284. [CrossRef]
[PubMed]
28. Gil, S.B.; Herrero, M.A.; Flores, M.C.; Pachoud, M.L.; Hellmers, M.M. Intensificación agropecuaria evaluada
por indicadores de sustentabilidad ambiental. Arch. Zootec. 2009, 58, 413–423. [CrossRef]
29. Rearte, D.H. La Producción de Carne en Argentina; INTA. Sitio Argentino de Producción Animal: Córdoba,
Argentina, 2007; pp. 1–25. Available online: http://www.produccion-animal.com.ar/informacion_
tecnica/origenes_evolucion_y_estadisticas_de_la_ganaderia/00-origenes_evolucion_y_estadisticas_de_
la_ganaderia.htm (accessed on 28 September 2018).
30. Frasinelli, C.A.; Veneciano, J.H. Introducción. In Sistemas Bovinos Sobre Gramíneas Megatérmicas Perennes en
San Luis; Frasinelli, C.A., Veneciano, J.H., Eds.; Ediciones INTA: Buenos Aires, Argentina, 2014; pp. 13–14,
ISBN 978-987-521-472-9.
31. Morris, C.D. Rangeland management for sustainable conservation of natural resources. In Grassland
Productivity and Ecosystem Services; Lemaire, G., Hodgson, J., Chabbi, A., Eds.; CABI: Wallingford, UK;
Cambridge, MA, USA, 2011; pp. 198–207, ISBN 978-1-84593-809-3.
32. Herrero, M.; Havlík, P.; Valin, H.; Notenbaert, A.; Rufino, M.C.; Thornton, P.K.; Blümmel, M.; Weiss, F.;
Grace, D.; Obersteiner, M. Biomass use, production, feed efficiencies, and greenhouse gas emissions from
global livestock systems. Proc. Natl. Acad. Sci. USA 2013, 110, 20888–20893. [CrossRef] [PubMed]
33. Schacht, W.H.; Reece, P.E. Impacts of livestock grazing on extensively managed grazing lands.
In Environmental Impacts of Pasture-Based Farming; McDowell, R.W., Ed.; CABI: Cambridge, MA, USA,
2008; pp. 122–143, ISBN 978-1845934118.
34. Pereira, H.M.; Leadley, P.W.; Proença, V.; Alkemade, R. Scharlemann, J.P.W.; Fernandez-Manjarrés, J.F.;
Araújo, M.B.; Balvanera, P.; Biggs, R.; Cheung, W.W.L.; et al. Scenarios for Global Biodiversity in the 21st
Century. Science 2010, 330, 1496–1501. [CrossRef] [PubMed]

137
Sustainability 2018, 10, 4228

35. DeRamus, H.A.; Clement, T.C.; Giampola, D.D. Dickison, P.C. Methane missions of beef cattle on forages:
Efficiency of grazing management systems. J. Environ Qual. 2003, 32, 269–277. Available online: https://pdfs.
semanticscholar.org/1d58/15b6d22d81070c173f6281434dd213a557c7.pdf (accessed on 28 September 2018).
[CrossRef] [PubMed]
36. Guzmán, M.L.; Sager, R. Inventario de metano entérico de los sistemas de producción de carne para San
Luis en el año 2009. Rev. Investig. Agropecu. 2013, 39, 88–94. Available online: http://www.scielo.org.ar/
pdf/ria/v39n1/v39n1a13.pdf (accessed on 28 September 2018).
37. Echeverría, J.C.; Giulietti, J. Precipitación media anual y temperatura del aire. In Aptitud Forestal de la
Provincia de San Luis: II Cartografía de Variables Ambientales; Echeverría, J.C., Jobbagy, E., Collado, A., Eds.;
INTA: San Luis, Argentina, 2006; pp. 11–13.
38. Peña Zubiate, C.; Anderson, D.L.; Demmi, M.A.; Saenz, J.L.; D’Hiriart, A. Carta de Suelos y Vegetación
de la Provincia de San Luis; Ediciones INTA: Buenos Aires, Argentina, 1998; pp. 1–116. Available
online: https://inta.gob.ar/sites/default/files/script-tmp-carta_de_suelos_hoja_san_luis.pdf (accessed on
28 September 2018).
39. Anderson, D.L.; De Aguilera, J.A.; Bernardon, A.E. Las formaciones vegetales de la provincia de San Luis.
Rev. Investig. Agropecu. 1970, 7, 153–183.
40. Riedel, J.L.; Frasinelli, C.A. Los sistemas de producción bovina de la provincia de San Luis, Argentina.
Oportunidades y desafíos. In Proceedings of the 3rd Simposio Internacional Sobre Producción Animal.
Utilización de forrajes en la Nutrición de Rumiantes, Temascaltepec de Gonzáles, México, 6–8 May 2013.
41. Cocimano, M.; Lange, A.; Menvielle, E. Equivalencias ganaderas para vacunos de carne y ovinos (escalas
simplificadas). In Colección Estudios y Métodos, 4th ed.; AACREA: Buenos Aires, Argentina, 1983; pp. 1–32.
42. IPCC. IPCC Guidelines for National Greenhouse Gas Inventories. Agriculture, Forestry and other Land Use;
Eggleston, H.S., Buendia, L., Miwa, K., Ngara, T., Tanabe, K., Eds.; Prepared by the National Greenhouse
Gas Inventories Programme; IGES: Kanagawa, Japan, 2006; Volume 4, Chapter 10; pp. 10.1–10.87,
ISBN 4-88788-032-4.
43. Forster, P.; Ramaswamy, V.; Artaxo, P.; Berntsen, T.; Betts, R.; Fahey, D.W.; Haywood, J.; Lean, J.; Lowe, D.C.;
Myhre, G.; et al. Changes in Atmospheric constituents and in radiative forcing. In Climate Change 2007: The
Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the IPCC; Solomon, S.,
Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L., Eds.; Cambridge
University Press: Cambridge, UK, 2008; Chapter 2; p. 234, ISBN 978-0521705967.
44. Cambra-López, M.; García Rebollar, P.; Estellés, F.; Torres, A. Estimación de las emisiones de los rumiantes
en España: El factor de conversión de metano. Arch. Zootec. 2008, 57, 89–101.
45. Aguilera, M. Uso ganadero de los pastizales naturales de San Luis. In Con las metas claras. La Estación
Agropecuaria San Luis. 40 años en favor del Desarrollo Sustentable; Aguilera, M.O., Panigatti, J.L., Eds.; Ediciones
INTA: Buenos Aires, Argentina, 2003; pp. 89–124, ISBN 978-9875210745.
46. National Research Council. Nutrient Requirements of Beef Cattle; Seventh Revised Edition: Update 2000; The
National Academies Press: Washington, DC, USA, 1996.
47. McCullagh, P.Y.; Nelder, J. Generalized Linear Models. Monographs on Statistics and Applied Probability 37, 2nd
ed.; Chapman and Hall: London, UK, 1989; pp. 1–512, ISBN 978-0412317606.
48. Burnham, K.P.; Anderson, D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic
Approach, 2nd ed.; Springer: New York, NY, USA, 2002; pp. 1–488, ISBN 978-0387953649.
49. Burnham, K.P.; Anderson, D.R.; Huyvaert, K.P. AIC model selection and multimodel inference in behavioral
ecology: Some background, observations, and comparisons. Behav. Ecol. Sociobiol. 2011, 65, 23–35. [CrossRef]
50. Tsegaye, D.; Haile, M.; Moe, S.R. The effect of land use on the recruitment and population structure of the
important food and fodder plant, Dobera glabra (Forssk.) Poir., in northern Afar, Ethiopia. J. Arid Environ.
2010, 74, 1074–1082. [CrossRef]
51. Manning, P.; Putwain, P.D.; Webb, N.R. Identifying and modelling the determinants of woody plant invasion
of lowland heath. J. Ecol. 2004, 92, 868–881. [CrossRef]
52. Zar, J.H. Biostatistical Analysis, 4th ed.; Pearson Prentice Hall: Upper Saddle River, NJ, USA, 1999;
ISBN 0130823902.
53. Hair, J.F., Jr.; Black, W.C.; Babin, B.J.; Anderson, R.E. Multivariate Data Analysis. A Global Perspective, 7th ed.;
Pearson: London, UK, 2006; pp. 1–785, ISBN 978-1292021904.

138
Sustainability 2018, 10, 4228

54. Garcia-Martinez, A.; Olaizola, A.; Bernues, A. Trajectories of evolution and drivers of change in European
mountain cattle farming systems. Animal 2009, 3, 152–165. [CrossRef] [PubMed]
55. IBM. IBM SPSS Advanced Statistics 20; IBM: Armonk, NY, USA, 2011.
56. Sheppard, S.C.; Bittman, S.; Donohoe, G.; Flaten, D.; Wittenberg, K.M.; Small, J.A.; Berthiaume, R.;
McAllister, T.A.; Beauchemin, K.A.; McKinnon, J.; et al. Beef cattle husbandry practices across Ecoregions of
Canada in 2011. Can. J. Anim. Sci. 2015, 95, 305–321. [CrossRef]
57. Modernel, P.; Astigarraga, L.; Picasso, V. Global versus local environmental impacts of grazing and confined
beef production systems. Environ. Res. Lett. 2013, 8, 035052. [CrossRef]
58. Nieto, M.I.; Guzmán, M.L.; Steinaker, D. Emisiones de gases de efecto invernadero: Simulación de un sistema
ganadero de carne típico de la región central Argentina. Rev. Investig. Agropecu. 2014, 40, 92–101.
59. Beauchemin, K.A.; Henry Janzen, H.; Little, S.M.; McAllister, T.A.; McGinn, S.M. Life cycle assessment of
greenhouse gas emissions from beef production in western Canada: A case study. Agric. Syst. 2010, 103,
371–379. [CrossRef]
60. Beukes, P.C.; Gregorini, P.; Romera, A.J.; Levy, G.; Waghorn, G.C. Improving production efficiency
as a strategy to mitigate greenhouse gas emissions on pastoral dairy farms in New Zealand.
Agric. Ecosyst. Environ. 2010, 136, 358–365. [CrossRef]
61. Bogaerts, M.; Cirhigiri, L.; Robinson, I.; Rodkin, M.; Hajjar, R.; Costa Junior, C.; Newton, P. Climate change
mitigation through intensified pasture management: Estimating greenhouse gas emissions on cattle farms in
the Brazilian Amazon. J. Clean. Prod. 2016, 162, 1539–1550. [CrossRef]
62. Casey, J.W.; Holden, N.M. Quantification of GHG emissions from sucker-beef production in Ireland.
Agric. Syst. 2006, 90, 79–98. [CrossRef]
63. Clark, H.; Pinares-Patiño, C.; De Klein, C. Methane and nitrous oxide emissions from grazed grasslands.
In Grassland: A Global Resource; McGilloway, D.A., Ed.; Wageningen Academic Publishers: Wageningen,
The Netherlands, 2005; pp. 279–293, ISBN 978-90-76998-71-8.
64. Beauchemin, K.A.; Janzen, H.H.; Little, S.M.; McAllister, T.A.; McGinn, S.M. Mitigation of greenhouse gas
emissions from beef production in western Canada—Evaluation using farm-based life cycle assessment.
Anim. Feed Sci. Technol. 2011, 166–167, 663–677. [CrossRef]
65. Veysset, P.; Lherm, M.; Bébin, D.; Roulenc, M.; Benoit, M. Variability in greenhouse gas emissions,
fossil energy consumption and farm economics in suckler beef production in 59 French farms.
Agric. Ecosyst. Environ. 2014, 188, 180–191. [CrossRef]
66. Legesse, G.; Beauchemin, K.A.; Ominski, K.H.; McGeough, E.J.; Kroebel, R.; MacDonald, D.; Little, S.M.;
McAllister, T.A. Greenhouse gas emissions of Canadian beef production in 1981 as compared with 2011.
Anim. Prod. Sci. 2016, 56, 153–168. [CrossRef]
67. Gerber, P.; Vellinga, T.; Opio, C.; Steinfeld, H. Productivity gains and greenhouse gas emissions intensity in
dairy systems. Livest. Sci. 2011, 139, 100–108. [CrossRef]
68. Bava, L.; Sandrucci, A.; Zucali, M.; Guerci, M.; Tamburini, A. How can farming intensification affect the
environmental impact of milk production? J. Dairy Sci. 2014, 97, 4579–4593. [CrossRef] [PubMed]
69. Moreau, J.; Delaby, L.; Duru, M.; Guerin, G. Advices given about the forage system: Evolutions and
conceptions concerning the steps to be taken and the tools to be used. Fourrages 2009, 200, 565–586.
70. Mugnier, S.; Magne, M.A.; Pailleux, J.Y.; Poupart, S.; Ingrand, S. Management priorities of livestock farmers:
A ranking system to support advice. Livest. Sci. 2012, 144, 181–189. [CrossRef]
71. Pinares-Patiño, C.S.; Waghorn, G.C.; Hegarty, R.S.; Hoskin, S.O. Effects of intensification of pastoral farming
on greenhouse gas emissions in New Zealand. N. Z. Vet. J. 2009, 57, 252–261. [CrossRef] [PubMed]
72. Pickering, N.K.; Oddy, V.H.; Basarab, J.; Cammack, K.; Hayes, B.; Hegarty, R.S.; Lassen, J.; McEwan, J.C.;
Miller, S.; Pinares-Patino, C.S.; et al. Animal board invited review: Genetic possibilities to reduce enteric
methane emissions from ruminants. Animal 2015, 9, 1431–1440. [CrossRef] [PubMed]
73. Berndt, A.; Tomkins, N.W. Measurement and mitigation of methane emissions from beef cattle in tropical
grazing systems: A perspective from Australia and Brazil. Animal 2013, 7, 363–372. [CrossRef] [PubMed]
74. Young, J.; Kingwell, R.; Bathgate, A.; Thomoson, A. Agricultural greenhouse gas emission reporting: The
implications for farm management. Agroecol. Sustain. Food Syst. 2016, 40, 261–276. [CrossRef]
75. Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science 2004, 304,
1623–1627. [CrossRef] [PubMed]

139
Sustainability 2018, 10, 4228

76. Follet, R.F.; Schuman, G.E. Grazing land contribution to carbon sequestration. In Grassland: A Global Resource;
McGilloway, D.A., Ed.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2005; pp. 265–277,
ISBN 978-90-76998-71-8.
77. Soussana, J.F.; Tallec, T.; Blanfort, V. Mitigation the greenhouse gas balance of ruminant production through
carbon sequestration in grasslands. Animal 2010, 4, 334–350. [CrossRef] [PubMed]
78. Schils, R.L.M.; Verhagen, A.; Aarts, H.F.M.; Sebek, L.B.J. A farm level approach to define successful mitigation
strategies for GHG emissions from ruminant livestock systems. Nutr. Cycl. Agroecosyst. 2005, 71, 163–175.
[CrossRef]
79. Pelletier, N.; Pirog, R.; Rasmussen, R. Comparative life cycle environmental impacts of three beef production
strategies in the upper midwestern United States. Agric. Syst. 2010, 103, 380–389. [CrossRef]
80. Zhuang, M.H.; Gongbuzeren; Li, W.J. Greenhouse gas emission of pastoralism is lower than combined
extensive/intensive livestock husbandry: A case study on the Qinghai-Tibet Plateau of China. J. Clean. Prod.
2017, 147, 514–522. [CrossRef]
81. Salvador, S.; Corazzin, M.; Romanzin, A.; Bovolenta, S. Greenhouse gas balance of mountain dairy farms as
affected by grassland carbon sequestration. J. Environ. Manag. 2017, 196, 644–650. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

140
 sustainability

Article
Effect of Three Husbandry Systems on Environmental
Impact of Organic Pigs
Gwendolyn Rudolph 1 , Stefan Hörtenhuber 1, *, Davide Bochicchio 2 , Gillian Butler 3 ,
Roland Brandhofer 1 , Sabine Dippel 4 , Jean Yves Dourmad 5 , Sandra Edwards 3 ,
Barbara Früh 6 , Matthias Meier 7 , Armelle Prunier 5 , Christoph Winckler 1 , Werner Zollitsch 1
and Christine Leeb 1
1 Department for Sustainable Agricultural Systems, University of Natural Resources and Life Sciences Vienna,
1180 Vienna, Austria; gwendolyn.rudolph@fibl.org (G.R.); [email protected] (R.B.);
[email protected] (C.W.); [email protected] (W.Z.); [email protected] (C.L.)
2 Research Centre for Animal Production and Aquaculture, Council for Agricultural Research and Economics,
41100 Modena, Italy; [email protected]
3 School of Natural and Environmental Sciences, Newcastle University, NE1 7RU Newcastle Upon Tyne, UK;
[email protected] (G.B.); [email protected] (S.E.)
4 Institute of Animal Welfare and Animal Husbandry, Federal Research Institute for Animal Health,
29223 Celle, Germany; sabine.dippel@fli.de
5 Physiology of Adaptation, Animal Nutrition and Health, INRA, 35590 Saint-Gilles, France;
[email protected] (J.Y.D.); [email protected] (A.P.)
6 Department of Extension, Training and Communication, FiBL, 5070 Frick, Switzerland;
barbara.frueh@fibl.org
7 Department of Socio-Economic Sciences, FiBL, 5070 Frick, Switzerland; matthias.meier@fibl.org
* Correspondence: [email protected]; Tel.: +43-1-47654-93229

Received: 29 September 2018; Accepted: 17 October 2018; Published: 20 October 2018

Abstract: This study examined the environmental impact of the three common organic pig husbandry
systems, indoor (n = 24), partly outdoor (n = 30), and outdoor (n = 10), in eight European countries.
Global warming (GWP), acidification (AP), and eutrophication potential (EP) was assessed per
1000 kg pig live weight on 64 farrow-to-finish pig production chains (cradle to farm gate). GWP, AP,
and EP varied greatly, and the most important source was feed production, followed by housing.
GWP did not differ between systems (p = 0.934), but AP in indoor systems and EP in outdoor systems
were higher than in partly outdoor systems (p = 0.006 and p = 0.010, respectively). The higher AP in
indoor systems can mainly be explained by NH3 arising from manure spreading, while PO4 -eq arising
from feed consumption and emissions on pasture accounted for the higher EP in outdoor systems.
Associations of farm characteristics with (reduced) environmental impacts were mainly found for
AP and EP, and included: (Increasing) farm size, numbers of piglets born and weaned per litter,
(bought-in) mineral feed, and high-protein by-products, the latter probably connected to beneficial
effects of appropriate dietary digestible lysine levels and feed conversion ratio. Increasing carcass
weights and dietary cereal proportions were associated with higher environmental impacts. Overall,
variation was mostly higher within than between systems, and measures to mitigate environmental
impact were identified.

Keywords: life cycle assessment; global warming potential; acidification potential; eutrophication
potential; cradle to farm gate; indoor; outdoor

Sustainability 2018, 10, 3796; doi:10.3390/su10103796 141 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3796

1. Introduction
Together with the general growth of organic farming in many European countries, organic pig
farming has expanded in recent decades [1]. However, the pig meat sector still ranks relatively low in
organic product sales, particularly in comparison to the sheep and bovine sectors [2].
Climate change as well as animal health and welfare are among the most current issues in the
public and scientific debate concerning livestock [3–6]. Likewise, sustainability and its assessment,
covering environmental, economic, and social aspects, have gained importance in recent years. For
instance, the Sustainability Assessment of Food and Agriculture systems (SAFA) Guidelines [7]
have been developed as an international reference document to allow for consistent analyses and
assessments despite the complexity of sustainability. According to the SAFA guidelines, sustainability
consists of four dimensions: Good governance, environmental integrity, economic resilience, and social
well-being. In the dimension of environmental integrity, the following themes are addressed:
Atmosphere, water, land, materials and energy, biodiversity, and animal welfare.
Livestock production exerts severe impacts on soil, water, and air quality due to the related
emissions [4]. The world’s livestock sector contributes 14.5% of global greenhouse gas emissions,
with pigs accounting for 9% of overall livestock-related emissions [5].
The life cycle assessment (LCA) provides a valuable and consistent methodological framework to
quantify the environmental impact within the life cycle of a product [8]. Hence, several LCAs have been
conducted in recent years to quantify the environmental impact, mainly greenhouse gas emissions
(global warming potential, GWP), acidification potential (AP), and eutrophication potential (EP),
of animal husbandry systems [9–11]. Until now, due to high CH4 emissions from enteric fermentation,
ruminants have mainly been in the focus, but in light of the high consumption of pork and pork
products in the European Union, pork production must also be considered.
Since pig production is dominated by non-organic production systems, most studies cover
conventional systems [4]. As for most LCA studies dealing with pigs, for organic pig production,
which is still comparatively small-scale, but nevertheless rapidly developing, only a few modelling
studies are available [12–14]. Only a few studies have conducted an LCA using individual farm
data [15], and even fewer have been based on a considerable number of organic farrow-to-finish
pig farms.
As organic pigs are produced according to the general principles of organic farming [16], national,
and international regulations (e.g., EC Nos. 2018/848 and 889/2008, [17,18]) as well as private
standards [19], organic pig farms have been treated as a uniform system in most studies. However,
it has recently been shown that organic pig farms in Europe can clearly be distinguished into three
main “husbandry systems”: Pigs may be kept completely outdoors in paddocks on pasture, as in
most UK and Italian farms, or indoors, with access to a limited concrete outside run, as in most farms
in German speaking countries. Furthermore, both systems, indoor and outdoor, may be combined
on one farm for different production stages or during different seasons, as is common, for example,
in Denmark or France [1,20].
Keeping pigs on pasture has a potentially higher risk regarding nutrient losses [14,21] compared
to pigs kept indoors, where manure is collected, stored, and spread in a controlled way on fields.
Furthermore, due to a more controlled (thermal) environment, pigs kept indoors might have better
feed conversion ratios and a higher number of piglets weaned, both reducing the environmental
impact [22,23].
Besides the effects on environmental impact caused by the husbandry system, as described above,
other important influencing factors contribute to variation. As LCA data from 27 conventional farms
show, other factors, such as diet characteristics (e.g., level of by-products), influence the environmental
impacts [9]. Therefore, also for organic pig production, individual farm data are needed to describe
and quantify the potential influence of the three husbandry systems as well as those individual farm
characteristics with potential impact on the environment.

142
Sustainability 2018, 10, 3796

Consequently, the present study aims to deliver first indications to support strategic decisions in
the organic sector (policy makers, extension services) or at the farm level (farmer). The analysis
focuses on the environmental impact of three common organic pig husbandry systems, indoor
(IN), partly outdoor (POUT), and outdoor (OUT), regarding their GWP, AP, and EP. Furthermore,
farm characteristics influencing these impacts are assessed by cluster and correlation analysis.
Two hypotheses are tested: (1) The null hypothesis that there are no differences between husbandry
systems regarding the environmental impact (GWP, AP, EP), and (2) that there are specific farm
characteristics, which explain variation independent from the husbandry systems.

2. Materials and Methods

2.1. Overall Study Design and Participating Farms

The present assessments are based on data collected during visits to 74 organic pig farms,
representing three different husbandry systems, IN (34 farms), POUT (28 farms), and OUT (12 farms),
in eight European countries (Austria, Czech Republic, Denmark, France, Germany, Italy, Switzerland,
and the United Kingdom) during 2012 and 2013 (see Supplementary Materials). In each country,
all assessments were carried out by one trained observer. All observers attended a common training
course to standardize assessments. The different husbandry systems were defined as described in
Table 1.

Table 1. Definition of the three organic pig husbandry systems: IN, POUT, and OUT.

System Abbreviation Definition 1,2

Pigs live in buildings with access to a concrete outside run, or to an
indoor IN outside run on soil, which is a small sacrifice area for permanent pig use
and not integrated into crop rotation.
Pigs spend part of the production cycle indoors and part outdoors.
There can be at least one production stage (dry sows, lactating sows,
partly
POUT group suckling, weaned piglets, or finishing pigs) outside while the rest
outdoor
is housed, or pigs spending part of the year outside and the rest indoors
(seasonal housing).
Pigs live permanently outdoors in paddocks with shelter (temporary
outdoor OUT hut or permanent building), but unrestricted access to the soil. The
paddock is usually integrated as pasture in a crop rotation.
1 Weaned piglets kept in an enclosure directly on soil in fields are considered OUT if only the lying area is roofed,
and considered IN if the entire enclosure is roofed; 2 if only a small percentage of the animals (<10% in herds of up
to 300 pigs in total, or <5% in larger herds) are kept in a different husbandry system, the farm is classified according
to the dominant system.

Organic pig farms were recruited through farm advisors, producer associations, agricultural
journals and their websites, or personal contacts. Farms had to be certified organic for at least two
years and preferably combined farrow-finish farms with more than 20 sows and 100 finishing places.
Recruitment was also based on the type of husbandry system, as the objective was to compare the
three different organic pig systems.
As this study investigated the environmental impact of pork production from piglet production
until slaughter, production chains from farrowing to finishing (PC) were the statistical unit. This
comprised 64 PCs (24 IN, 30 POUT, 10 OUT), which were either farrow-to-finish farms (15 IN, 24 POUT,
9 OUT) or which were formed of co-operating farrowing-only and fattening-only farms (6, 6, and
1 IN, POUT and OUT PCs, respectively). Additionally, for three other PCs (IN), data from the
co-operating farm was not available during the study, and the average of the other farms was then
used for the missing part of the PC. For each individual PC, environmental impact categories were
calculated as outlined below, with pairs of farrowing-only and fattening-only farms being treated as
farrow-to-finish farms.

143
Sustainability 2018, 10, 3796

Based on the literature [10,15,24] and expert knowledge, a standardized on-farm assessment
protocol for use on a tablet computer was developed and a supplementary dictionary was translated to
the languages of involved countries. The final protocol included an interview with the farm manager,
the analysis of farm records, and direct observations. It was structured in thematic sections, including
the following parameters:

• Farm and manure management, description of husbandry systems;

• productivity data and medicinal treatments (records);
• land use (crop production);
• diet composition and dietary nutrients contents; and
• provision of resources (husbandry system) for weaners (defined as pigs from post weaning with at
least six weeks until transfer to a fattening unit with approximately 12 weeks), fatteners (includes
the growing and finishing phase from approximately 30 kg to slaughter), pregnant, and lactating
sows (direct observations)

The PC-specific data used in the present study are based on inventory data either collected on the
day of visit or covering a period of 12 months prior to the farm visits.

2.2. Scope of the Study and Life Cycle Assessment Methodology

2.2.1. System Boundaries, Functional Unit, and Allocation Approach

As the study focused on pig farming systems, transport, slaughter, and processing of the carcasses
were not included. The system boundaries were defined as cradle-to-farm gate, in this case from piglet
birth to pigs ready for slaughter, and included relevant farm inputs needed for this (e.g., electricity,
transport-related (fossil) energy for feedstuffs, etc.). While the energy-gain from co-digestion of manure
in biogas plants was not considered (as not directly related to the pig unit), digestion-related emission
factors were used to derive results from co-digestion of manure. Following LCA-related guidelines,
such as PAS2050 [25], for the assessment of greenhouse gas emissions, emissions from the construction
of farm infrastructure (e.g., livestock barns, machinery, farm buildings) were excluded from the
LCA. Furthermore, veterinary treatments and inputs, such as cleaning agents and disinfectants, were
not considered within the system boundaries as a lower use is assumed in organic farming [26].
The functional unit was 1000 kg of live weight of fattening pigs leaving the farm (live weight at
slaughter), including culled sows. The live weight at slaughter was calculated based on carcass weight
records using an equation used for organic pigs from different countries [27]. An energy allocation
approach was used throughout the study, for instance, for feedstuffs’ emission factors.

2.2.2. Environmental Impacts Considered, Data Sources, and Methodological Details

GWP (100 year-horizon) [28], AP, and EP were calculated using a modified version of an Excel
tool developed by Dourmad et al. [15]. Emissions were calculated from measured as well as modelled
data per individual PC, using typical emission factors for livestock-related emissions [29]. For EP
and AP from the pig unit and feed production, characterization factors were used as described in [8]
and [30]. Gaseous emissions from animal husbandry and manure storage were calculated for NH3 ,
N2 O, and NOX as well as CH4 based on [28,29,31] and other sources as described in [15].
Calculations for nitrogen (N) and phosphorous (P) retention and excretion have been described in
detail in [29,32]. Results from [33], adapted according to [34], were used to estimate losses from outdoor
paddocks into water, assuming a constant rate between P losses and the body mass (live-weight) of
pigs on pasture (see Equation (S1) in the Supplementary Materials). P losses from manure storage,
treatment, and spreading were assumed to be negligible and ignored [29]. All emission factors used
are given in the Supplementary Material. All traits used for deriving the indicators of the pig unit’s
environmental impact are provided in Table 2.

144
Sustainability 2018, 10, 3796

Table 2. Input data for the characterization of the environmental impact of organic pig systems.

Category Parameter
sow number of weaned piglets per sow and year, replacement rate (%), live weight at slaughter
performance (kg), feed intake during gestation and lactation (kg/period), duration of lactation (days)
weaner weight at weaning (kg), piglet mortality (%), daily feed intake (kg), feed conversion rate
performance (kg feed/kg live weight gain), duration of weaning period (days)
weight at beginning of fattening phase (kg), mortality (%), daily feed intake (kg), feed
fattener
conversion rate (kg feed/kg live weight gain), daily weight gain (kg/day), live weight at
performance
slaughter (kg), age at slaughter (days), duration of fattening period (days)
diet composition (% of individual feed ingredients), diet nutrient, i.e., crude protein (CP, g/kg)
diets
and phosphorus (P, g/kg), and metabolizable energy content (MJ/kg)
land use on-farm crop production
animal type of system, i.e., outdoor (OUT), partly outdoor (POUT), indoor (IN) with outside run, type
husbandry of floor (solid floor, slats/partly slatted, deep litter)
manure type (liquid, solid), manure handling (cleaning frequency), manure storage (type and
duration), manure treatment (composting, anaerobic/aerobic digestion), type and distance of
manure
spreading (wide spreading, injection), mean distance of manure transport to place of
spreading, crop rotation, and stocking rate (animals/ha)
very good: 100% of litter is clean, dry, and not mouldy
bedding good: >50% of litter is clean, dry, and not mouldy
quality poor: >50% of litter is dirty, wet, or mouldy
very poor: 100% of litter is dirty, wet, or mouldy

Parameters to calculate the environmental impact from the production of all feedstuffs, except
fishmeal and fish oil, were adopted from previous studies [35,36]. The nitrogen (N)-related part of feeds’
EP was calculated by multiplying typical quantities of N applied in manure and commercial fertilizers
on organic farms in Austria with typical NO3 -N leaching factors identified in [37]. For P-losses from
feed production, it was assumed that, on average, a surplus of 5% over plant requirements (according
to yield) was applied and lost. The GWP of the rarely used components, fishmeal and fish oil, originate
from [38]. The GWP, AP, and EP for monocalcium phosphate and mineral premixes are based on the
Danish LCA food database [39].
The total feed consumption per animal, including bought–in-feedstuffs, was calculated from
farm-specific data (based on daily consumption per animal, feed conversion rate, duration of the
periods, average daily gains, etc.). For individual missing values, results from [40] and [41] were
used in the fattening and the weaner stages, respectively. For farms lacking full records on the
feed intake and feed conversion ratio, these values were estimated according to farm and animal
category-specific dietary contents for MJ ME, CP, and P, and recommended nutrient requirements
at the respective physiological stage [42]. Furthermore, the relative amount of digestible lysine per
unit of energy (g/MJ NE) was calculated based on the online tool, Evapig [43], and compared to
requirements at different stages [44]; a 10% tolerance was accepted due to the uncertainty of NE and
lysine content. Diets for growing and finishing pigs were classified as sufficient, deficient, or exceeding
requirements (excess) using the content of digestible lysine relative to the NE content as an indicator.
Feed components and feedstuffs were categorized as described in Table 3.

2.2.3. Characteristics of the Husbandry Systems

Animal Performance, Production Data, and Feeding Characteristics

Animal performance and production data, as well as feed characteristics, varied substantially
within and between systems, see Supplementary Materials (Tables S4 and S5). In OUT-PCs, the number
of piglets born and weaned per sow was lower than in the other systems, but the median age at culling
was higher, and hence the replacement rate was lower in OUT. OUT-PCs showed lower mortality and

145
Sustainability 2018, 10, 3796

heavier pigs at weaning. Some of the diverging characteristics, such as numerically smaller sows in
OUT, are probably related to the use of local, traditional breeds (e.g., Cinta Senese, Tamworth). Median
live weight (kg) of slaughter pigs was 131.0 kg in IN, 117.0 kg in POUT, and 124.0 kg in OUT. Diet
characteristics and amounts of feed used differed in many parameters between the husbandry systems.
However, average metabolizable energy and crude protein contents were similar between systems for
sow diets, and similar average metabolizable energy were recorded for weaners and finishing farms.

Table 3. Categorization of feed components and feedstuffs.

Feed Stuff Category Component

animal or microbial origin brewer’s yeast, fish meal, fish oil, whey powder (sweet), whey concentrate
compound feed different compound feeds for growing and/or finishing pigs
grains (cereals) barley, maize, rye, oat, triticale, wheat
false flax seed cake, potato protein, rapeseed cake, rapeseed meal,
high-protein by-products
sunflower seed cake
leguminous grains fava beans, peas, soybean, soybean cake
minerals clay, mineral premix, monocalcium phosphate
alfalfa (lucerne) green meal or similar roughage, brewer’s grains (dried),
others (based on processing of
grass cobs, rapeseed oil, spelt husks, sugar beet molasses, sunflower seed
plant raw materials)
oil, wheat bran, wheat starch
supplementary compound feed high-protein supplements

Housing (Floor Type) and Manure Management

The housing, and consequently the manure management, varied only between the individual
PCs in IN and POUT, while in OUT, all animals were kept outdoors. Detailed information on housing
(floor type) is provided for all animal categories in IN and POUT-PCs in the Supplementary Materials
(Table S6). All animal categories in IN were kept on (partly slatted) concrete floors, with bedded lying
areas. For POUT, 83% of PCs kept lactating sows outdoors throughout the year, and 45% kept dry
sows outside, with a much lower proportion keeping weaners and fatteners outdoors.
The floor types for weaners and fatteners housed on POUT farms varied largely. Depending
on the floor type, IN and POUT PCs produced either solid manure only or solid manure and slurry.
In IN, 95.5% of the PCs generated a combination of solid manure and slurry, while only 4.5% had only
solid manure. In POUT, the proportion of PCs with both solid manure and slurry was 69%. In OUT,
no manure was stored and handled.
The type and frequency of manure treatments by husbandry system are reported in the
Supplementary Material (Table S7). In IN, 16.6% of PCs used aerobic digestion. Thirty percent
of the POUT-PCs applied a treatment (composting, aerobic, or anaerobic digestion) to the slurry.
Across all systems, most PCs did not treat the solid manure before application; composting was the
only treatment found on 26.3% of IN- and 15.3% of POUT-PCs.

2.3. Statistical Data Analysis

All statistical analyses were performed with each individual PC as the statistical unit in SAS 9.2
and 9.3 (SAS-Institute, Cary, North Carolina, USA, 2008). Non-parametric Kruskal-Wallis tests were
used for comparisons between husbandry systems. When significant effects (p < 0.05) were revealed
in global tests, pairwise comparisons were performed using the Wilcoxon Two-Sample (Rank sum)
test. p-Values were adjusted for multiple comparisons using Bonferroni correction. Additionally, to
investigate associations between the environmental impact categories of AP, EP, and GWP and farm
characteristics, Spearman rank correlations were calculated. Only those characteristics were included
which were not directly considered in the LCA calculation, except for piglets weaned per sow per year
[n, 1 yr mean] and carcass weight [kg, 1 yr mean].

146
Sustainability 2018, 10, 3796

Since AP, EP, and GWP did not significantly correlate with each other, they were subjected to a
hierarchical cluster analysis using the average linkage method. Values were standardized using the
procedure, STDIZE, in SAS using the mean as a location measure and the sample standard deviation as
a scale measure. For this analysis, five outliers (2 IN, 2 POUT, 1 OUT) were excluded, as identified from
boxplots, resulting in 59 PCs being included in the final cluster analysis. The number of clusters was
based on R-Squared (SAS-Institute, 2008), Pseudo F, and Pseudo t2 statistics. Additionally, the average
distance between the clusters was graphically checked in a dendrogram.

3. Results

3.1. GWP, AP, and EP of the Three Husbandry Systems

The total environmental impacts (AP, EP, and GWP) of the 64 PCs in the different husbandry
systems are presented in Table 4. Statistical comparison of the three pig husbandry systems with
respect to GWP, AP, and EP revealed inconsistent results.

Table 4. Environmental impact (global warming, GWP; acidification potential, AP; eutrophication
potential, EP) of organic pig production in three husbandry systems, IN, POUT, and OUT.

Husbandry n
Parameter Min. Q25% Median Q75% Max.
System (PC)
IN 24 1605 1860 2204 2347 2962
kg CO2 -eq/1000 kg live
GWP POUT 30 1663 1997 2213 2407 3393
weight at slaughter
OUT 10 1470 1593 2210 2705 3480
IN 24 38.0 55.2 61.9a 78.4 114.4
kg SO2 -eq/1000 kg live
AP POUT 30 37.8 47.0 51.9 b 61.0 88.4
weight at slaughter
OUT 10 34.8 38.4 55.4 ab 72.3 91.0
IN 24 13.6 18.2 21.6 ab 25.7 48.7
kg PO4 -eq/1000 kg live
EP weight at slaughter
POUT 30 13.3 17.8 20.1 b 25.1 43.2
OUT 10 17.8 19.9 28.7 a 36.8 46.2
a,bDifferent superscript letters indicate differences between groups for which p < 0.05 (p-values adjusted according
to Bonferroni correction for triple testing).

No significant differences were found regarding the GWP between systems. With 2204, 2213,
and 2209 kg CO2 -eq per 1000 kg live weight at slaughter, the median estimate for the GWP was similar
for the three systems, IN, POUT, and OUT (p = 0.934). Across systems, the PCs with the lowest and
highest GWP were both found in OUT, and the variation in the GWP was numerically smaller in IN
and POUT than in OUT.
In all systems, feed production most strongly contributed to the GWP, followed by animal housing
(direct emissions originating from the animal and excreta inside houses), and, in IN and POUT, manure
storage (Figure 1). Manure treatment and manure spreading contributed only a small percentage to
the GWP in IN and POUT, while in OUT, manure is directly excreted onto the field by the animal and
therefore is neither stored, treated, nor spread. Relative contributions of housing emissions tended
to be lower in IN, whereas the relative contribution of manure storage was highest for this system.
Consistently, the highest relative contribution of housing (including field deposition of manure) was
found for OUT.
The median AP was significantly higher in IN (61.9 kg SO2 -eq per 1000 kg live weight at slaughter)
than in POUT (51.9 kg SO2 -eq per 1000 kg live weight at slaughter; p = 0.006), mainly due to more
NH3 arising from manure spreading in IN. In OUT, AP was numerically slightly higher than in POUT.
Across systems, the individual PC with the lowest AP was found in OUT and the one with the highest
AP was in IN. The variation (interquartile range) was smaller in POUT compared to IN and OUT.
Similar to GWP, feed production and animal housing contributed most to AP (Figure 1). The
relative contribution of manure spreading in IN and POUT to both AP and EP was higher than the

147
Sustainability 2018, 10, 3796

corresponding contributions to GWP. Regarding AP, IN showed higher relative amounts of SO2 -eq
originating from feed, housing of the animals (direct emissions), and, especially, manure storage and
spreading. In POUT, some manure remains directly on the paddock and is not stored or spread on
the field, thus leading to lower AP due to lower NH3 emissions. Manure spreading was the main
explanation for differences in the AP between IN and POUT. An even higher difference was found
between OUT and IN, again due to the lack of manure spreading in OUT.

Figure 1. Mean relative contribution of the different sources to GWP, AP, and EP based on data from
IN (n = 24), POUT (n = 30), and OUT (n = 10) production chains.

The median EP, expressed in kg PO4 -eq per 1000 kg of live weight at slaughter, was significantly
higher in OUT than in POUT (p = 0.010), mainly due to more PO4 -eq resulting from feed consumption
and housing. Total EP of IN was similar to the EP of POUT, but did not differ significantly from
OUT. Variation (interquartile range) in OUT was larger than in the other systems. Across all systems,
the most important source of EP was feed production, followed by animal housing. In IN and POUT,
manure storage, treatment, and spreading also contributed to EP, but to a lesser extent. The highest
contribution of feed and housing regarding EP was found in OUT, which had a higher median feed
conversion rate than POUT- or IN-PCs, and consequently needed more feed to achieve 1000 kg of
slaughter weight.
When considering the environmental impact indicators (GWP, AP, EP) based on animal production
stages, across all systems the fattening phase had the highest influence (between 68% and 74% of the
totals), with little variation between the systems and impact indicators (Figure 2).

Figure 2. Mean relative contribution of the different animal categories to GWP, AP, and EP based on
data from IN (n = 24), POUT (n = 30), and OUT (n = 10) production chains.

3.2. Correlations between Farm Characteristics and Environmental Impacts

Correlation coefficients of farm characteristics with environmental impact indicators are presented
in Table 5. Two characteristics relating to size of the pig units (number of slaughtered pigs and
livestock units per PC) negatively correlated with AP and EP, with larger PCs having lower AP and EP.
The current number of sows on the farm, which also relates to farm size, was also negatively correlated
with AP.
148
Sustainability 2018, 10, 3796

Table 5. Coefficients of correlation (Spearman’s Rho’s) between farm characteristics (rows) and
environmental impact indicators (columns) for 61 production chains (three production chains had to
be excluded due to a missing animal category at the farm).

Parameter GWP AP EP
n sows [present at visit] ns −0.33 ** ns
slaughtered finishers [n/1 yr] ns −0.30 * −0.31 *
Livestock Unit ns −0.37 ** −0.30 *
piglets born per litter (life born + still born) [n, 1 yr mean] ns ns −0.44 ***
number of weaned piglets per sow per year −0.35 ** −0.27 * −0.37**
carcass weight [kg, 1 yr mean] ns 0.30 * 0.30*
age at culling [n farrowings] ns ns ns
Mastitis Metritis Agalactia (MMA) treatment of sows (%) ns ns ns
percentage of bought-in feed for finishers (%) ns −0.40 ** ns
grains (Cereals) ns ns 0.29 *
leguminous crops ns ns ns
high-protein by-products ns ns −0.26 *
relative contribution of others ns ns ns
feed stuff category (%) components of animal or microbial origin ns ns ns
minerals ns ns −0.40 **
compound feed ns ns ns
supplementary compound feed ns ns ns
ns: Not significant, * p < 0.05, ** p < 0.01, *** p < 0.001.

The total number of piglets born per litter negatively correlated with EP, whilst piglet numbers
weaned per sow and year negatively correlated with all environmental impact indicators. The average
final carcass weight correlated positively with AP and EP, while the percentage of bought-in feed
in fattener diets was negatively associated with AP. Additionally, the relationship between the
relative contribution of feedstuff categories to the diets and the environmental impact indicators
was investigated, but associations were only found for EP. The relative contribution of the high-protein
by-product feed and mineral supplements negatively correlated with EP, while the amount of grains
correlated positively.

3.3. Cluster Analysis Regarding Impacts of Organic Pig Husbandry Systems

The hierarchical cluster analysis revealed two suitable classification levels, with five and
four clusters, respectively. For statistical reasons (number of observations per cluster), the higher
aggregation level, i.e., combining clusters 1 and 4 to cluster 1/4, was chosen. The number of PCs per
husbandry system and cluster are shown in Table 6.

Table 6. Number of production chains per system (IN, POUT, OUT) in the four clusters identified.

Number of Production Chains Per System in Cluster

System Cluster 1/4 * Cluster 2 * Cluster 3 * Cluster 5
Impact Intermediate Low High Highest
IN 5 8 9 0
POUT 13 10 5 0
OUT 4 3 0 2
total 22 21 14 2
* Clusters subjected to further statistical analysis.

In Table 7 all clusters are presented: Cluster 2, representing 35.6% of the total, on average, showed
numerically the lowest environmental impacts (referred to as “low impact cluster” below). Cluster 1/4
can be considered as the “intermediate impact cluster”, with values of AP, EP, and GWP between those
of Cluster 2 and Cluster 3. Cluster 3 had higher median values for AP, EP, and GWP as compared

149
Sustainability 2018, 10, 3796

to Cluster 1/4 and Cluster 2. Consequently, Cluster 3 can be described as the “high impact cluster”.
Cluster 5 resulted in overall highest environmental impacts, but due to the very small number of farms,
included data are only presented descriptively, but not further considered in the analysis.

Table 7. Environmental impacts (GWP, AP, and EP) per 1000 kg of live weight at slaughter by cluster
(total N = 59 production chains) (cluster 5 not subjected to further statistical tests is highlighted in grey).

Parameter Cluster Number n (PC) Min. Q25% Median Q75% Max.

1/4 22 2008 2153 2222 2405 2962
GWP [kg CO2 -eq per 1000 kg 2 21 1470 1668 1776 1906 2102
live weight at slaughter] 3 14 1977 2316 2348 2416 2695
5 2 2705 2705 2908 3111 3111
1/4 22 46.0 51.9 56.0 59.0 63.3
AP [kg SO2 -eq per 1000 kg 2 21 34.7 40.0 47.0 50.9 59.1
live weight at slaughter] 3 14 69.5 72.1 77.3 81.2 88.2
5 2 72.3 72.3 74.1 76.0 76.0
1/4 22 15.8 19.7 21.1 24.6 29.1
EP [kg PO4 -eq per 1000 kg 2 21 13.3 17.0 17.6 18.6 20.5
live weight at slaughter] 3 14 22.7 24.8 25.9 28.0 30.5
5 2 36.8 36.8 37.5 38.1 38.1

Generally, environmental impact indicators were predominantly influenced by emissions from

feed and housing (direct emissions during animal keeping). Numerically, the low impact cluster had
the lowest contributions from these sources and Cluster 5 the highest.
Regarding GWP, the intermediate and high impact clusters had relatively comparable values,
which were slightly higher in the high impact cluster, but the contribution of the different sources to
total GWP differed numerically; the intermediate impact cluster was characterized by higher amounts
from feed and housing, while the contribution of manure storage and spreading was higher in the high
impact cluster. Considering AP and EP, the main difference leading to numerically higher amounts in
the high impact cluster compared to the intermediate impact cluster, were emissions from manure
spreading (Figure 3).

Figure 3. Mean relative contribution of the different sources to GWP, AP, and EP by cluster (total n = 59).
CL2 = Cluster 2 (low environmental impact cluster, n = 21), CL3 = Cluster 3 (high environmental impact
cluster, n = 14), CL5 = Cluster 5 (n = 2), CL1/4 = Cluster 1/4 (intermediate environmental impact
cluster, n = 22).

Median numbers of sows, livestock units, and finishing pigs slaughtered per year per cluster
ranged between 28 and 110, 38 to 121, and 324 to 859, respectively. These characteristics relating to
farm size were numerically lowest for the high impact cluster, while the highest values were found
in the intermediate impact cluster. The values for the low impact cluster were between those for the
intermediate and high impact cluster. There were, however, no statistical differences between impact
clusters in these parameters (see Supplementary Materials, Table S8).

150
Sustainability 2018, 10, 3796

The average weight of pigs at the end of the post-weaning period differed between clusters as
shown in Table 8. In the intermediate impact cluster, pigs entering the finishing phase were heavier
than in the high impact cluster (p = 0.012). Lower weights at the start of the fattening phase had a
negative effect on environmental impact indicators. Feed conversion for fattening pigs in the low
impact cluster was lower than in the intermediate and high impact clusters (p < 0.001). In line with
this, the total amount of feed per finished pig was lower in the low impact cluster in comparison to the
high impact cluster (p < 0.001) and to the intermediate impact cluster (p = 0.006; Table 9). Improved
feed conversion and lower feed consumption in the low impact cluster had a beneficial effect on
environmental impacts. However, mortality of finishers was higher in the low impact cluster than
in the high impact cluster (p < 0.001; Table 8). The percentage of bought-in feed in finishing diets
(Table 9) was lower for the high impact cluster in comparison to the low impact cluster (p = 0.000) and
the intermediate impact cluster (p < 0.001). Additionally, in the low and high impact cluster, more
leguminous grains were fed than in the intermediate impact cluster (Table 10).

Table 8. Characteristics of the animal categories by cluster.

Cluster impact
Animal n
Category [Cluster Min. Q25% Mean Median Q75% Max.
Category/Parameter 3 (PC)
Number]
sows
piglets born per litter low [2] 19 12.0 12.1 13.2 13.3 14.0 14.5
(live born + still born) intermediate [1/4] 20 6.0 10.8 12.1 12.3 14.0 16.5
[n, 1 yr mean] 1 high [3] 13 8.0 12.0 12.8 13.3 14.0 14.5
piglets weaned per low [2] 20 10.0 18.2 19.2 19.9 21.1 25.0
sow per year intermediate [1/4] 22 10.0 16.0 18.3 19.0 21.0 23.8
[n, 1 yr mean] 2 high [3] 14 14.0 16.0 18.3 19.1 19.7 25.0
low [2] 20 12.0 26.0 31.8 30.5 35.0 50.0
sow replacement rate
intermediate [1/4] 22 8.0 20.0 32.5 28.0 45.0 87.0
[%, 1 yr mean] 2
high [3] 14 20.0 20.0 29.0 26.5 33.0 53.0
low [2] 20 187 200 237 240 257 310
live weight at culling
intermediate [1/4] 22 180 220 249 245 275 325
[kg at culling] 2
high [3] 14 197 200 234 233 253 277
Weaners
low [2] 20 0.0 10.0 11.3 10.7 13.5 22.0
weight at weaning
intermediate [1/4] 22 5.5 10.0 13.1 12.5 15.0 28.0
[kg, 1 yr mean] 2
high [3] 14 8.0 10.0 11.5 10.9 12.5 22.0
weight at end of low [2] 20 24.0 25.8 29.4 30.0 ab 30.0 42.0
post-weaning intermediate [1/4] 22 25.0 30.0 31.6 31.5 b 35.0 40.0
[kg, 1 yr mean] 2 high [3] 14 23.0 25.0 28.3 29.0 a 30.0 34.0
mortality rate low [2] 20 0.0 3.5 5.7 5.0 5.0 20.0
weaners intermediate [1/4] 22 0.0 1.0 3.2 3.0 5.0 10.0
[%, 1 yr mean] 2 high [3] 14 0.0 1.0 3.1 3.0 5.0 5.0
fattening pigs
live weight at low [2] 20 104 112 124 117 129 165
slaughter intermediate [1/4] 21 86 112 128 120 136 200
[kg, 1 yr mean] 2 high [3] 14 116 121 131 129 140 150
mortality rate low [2] 20 1.0 1.5 2.9 3.0 a 4.0 5.0
fattening pigs intermediate [1/4] 21 0.0 1.0 1.9 2.0 ab 2.0 6.0
[%, 1 yr mean] 2 high [3] 14 0.0 0.0 1.0 1.0 b 1.0 4.0
1 Number of observations differs from number of production chains, as each parameter was not always assessable
for all farms; 2 number of observations differ from number of production chains, as the environmental impact
was calculated using mean values for missing animal categories for three farms (piglet production for two farms;
fattening pigs for one farm); 3 parameters that showed significant differences between clusters are printed in
bold; a,b different superscript letters indicate differences between groups (p < 0.05, p-values adjusted according to
Bonferroni correction for triple testing).

151
Sustainability 2018, 10, 3796

Table 9. Dietary characteristics by cluster.

Animal Category/ Cluster Impact Category n

Min. Q25% Mean Median Q75% Max.
Parameter 1 [cluster Number] (PC)
sows
low [2] 20 675 1028 1415 1458 1595 2053
feed per sow
intermediate [1/4] 22 827 1332 1603 1702 1834 2236
[kg/year]
high [3] 14 1060 1203 1383 1385 1473 1946
average dietary content of
low [2] 20 9.6 11.9 12.1 12.5 12.9 13.1
ME [MJ//kg] intermediate [1/4] 22 12.0 12.3 12.7 12.7 12.9 13.7
high [3] 14 11.8 12.4 12.6 12.6 13.0 13.3
low [2] 20 124 148 155 155 164 185
CP [g/kg] intermediate [1/4] 22 112 137 149 152 162 180
high [3] 14 133 146 150 151 157 165
low [2] 20 3.0 4.7 5.2 5.5 5.9 7.8
total P [g/kg] intermediate [1/4] 22 3.1 4.5 5.4 5.8 6.1 6.5
high [3] 14 3.3 4.4 5.0 5.3 5.5 6.0
Weaners
feed per weaner low [2] 20 18 30 38 39 45 56
produced intermediate [1/4] 22 12 33 43 38 50 111
[kg/weaner] high [3] 14 20 30 37 36 45 59
average dietary content of
low [2] 20 9.5 12.5 12.4 12.8 13.1 13.4
ME [MJ//kg] intermediate [1/4] 22 12.0 12.6 12.9 12.9 13.2 13.6
high [3] 14 12.0 12.9 13.0 13.1 13.4 13.5
low [2] 20 138 168 177 179 189 203
CP [g/kg] intermediate [1/4] 22 112 170 176 181 195 208
high [3] 14 147 172 180 182 188 208
low [2] 20 3.5 3.8 5.2 5.7 6.0 6.8
total P [g/kg] intermediate [1/4] 22 3.1 5.5 5.6 6.0 6.2 6.9
high [3] 14 3.5 4.7 5.5 5.5 5.8 8.9
Fattening pigs
low [2] 20 209 222 269 242 a 322 378
feed per fattening
intermediate [1/4] 21 159 266 381 337 ab 385 981
pig [kg]
high [3] 14 291 323 384 390 b 443 494
percentage of low [2] 18 20 58 79 100 a 100 100
bought-in feed stuff intermediate [1/4] 19 30 100 87 100 a 100 100
in fattener diets high [3] 14 0 7 35 25 b 69 100
low [2] 20 2.4 2.7 2.9 2.8 a 3.0 3.3
fattening pig FCR
intermediate [1/4] 21 3.0 3.2 3.8 3.6 b 4.2 6.0
[kg feed/kg pig]
high [3] 14 3.1 3.3 3.7 3.8 b 4.0 4.6
average dietary content of
low [2] 20 9.5 12.5 12.3 12.8 12.9 13.2
ME [MJ//kg] intermediate [1/4] 21 12.0 12.6 13.0 12.9 13.2 14.5
high [3] 14 12.0 12.7 13.0 12.9 13.0 14.8
low [2] 20 139 153 163 165 172 190
CP [g/kg] intermediate [1/4] 21 112 144 162 171 183 202
high [3] 14 118 153 157 158 164 177
low [2] 20 2.4 3.6 4.5 4.9 5.1 6.0
total P [g/kg] intermediate [1/4] 21 3.1 4.0 5.0 5.5 5.8 6.4
high [3] 14 3.3 4.0 4.6 4.8 5.1 6.0
1 Parameters that showed significant differences between clusters are highlighted in bold; a,b different superscript
letters indicate differences between groups (p < 0.05, p-values adjusted according to Bonferroni correction for
triple testing).

152
Sustainability 2018, 10, 3796

Table 10. Dietary proportion of feedstuff categories by cluster.

Cluster Impact Category n

Feed Category 1 Min. Q25% Mean Median Q75% Max.
[Cluster Number] (PC)
low [2] 19 0.0 50.0 53.2 61.8 67.8 74.5
cereal grains intermediate [1/4] 21 0.0 50.0 53.8 65.0 71.4 90.0
high [3] 14 41.4 65.0 67.2 68.1 71.8 85.5
low [2] 19 0.0 16.4 20.9 25.0 ab 27.5 31.6
leguminous
grains
intermediate [1/4] 21 0.0 7.5 16.3 17.4 b 21.9 44.4
high [3] 14 14.5 20.5 26.0 23.1 a 31.0 44.5
low [2] 19 0.0 2.0 5.3 4.7 8.4 13.1
high-protein
intermediate [1/4] 21 0.0 0.0 3.3 1.1 4.2 13.8
by-products
high [3] 14 0.0 0.0 2.7 1.6 6.4 6.9
low [2] 19 0.0 0.0 7.2 3.0 6.8 80.2
others intermediate [1/4] 20 0.0 0.0 3.9 0.1 5.1 17.1
high [3] 14 0.0 0.0 1.0 0.0 1.1 5.1
components of low [2] 19 0.0 0.0 0.4 0.0 1.0 3.2
animal or intermediate [1/4] 21 0.0 0.0 2.3 0.0 0.0 42.3
microbial origin high [3] 14 0.0 0.0 0.0 0.0 0.0 0.0
low [2] 19 0.0 2.0 2.6 2.7 3.1 5.4
minerals intermediate [1/4] 21 0.0 0.0 1.6 1.6 2.8 5.6
high [3] 14 0.0 2.0 2.2 2.4 2.9 4.0
low [2] 19 0.0 0.0 10.5 0.0 0.0 100
compound feed intermediate [1/4] 21 0.0 0.0 19.1 0.0 0.0 100
high [3] 14 0.0 0.0 0.0 0.0 0.0 0.0
low [2] 19 0.0 0.0 0.0 0.0 0.0 0.0
supplementary
intermediate [1/4] 21 0.0 0.0 0.0 0.0 0.0 0.0
compound feed
high [3] 14 0.0 0.0 1.0 0.0 0.0 11.4
1 Parameters that showed significant differences between clusters are printed in bold; a,b different superscript letters

within columns indicate differences between groups (p < 0.05, p-values adjusted according to Bonferroni correction
for triple testing).

The high impact cluster showed a higher proportion of PCs feeding sufficient digestible lysine to
finishing pigs, compared to the intermediate impact cluster (64.3% vs. 6.3%, respectively; p = 0.001;
Table 11). There were no differences in the proportion of deficient or excess diets for growing and
finishing pigs, but the low impact cluster still showed a high proportion of diets with sufficient
digestible lysine content (41.2%). Across the growing and finishing diets, the low impact cluster
showed the highest proportion of diets without deficient digestible lysine (82.4%).

Table 11. Classification of animal categories by cluster according to deficient, excess, or sufficient
proportions of digestible lysine in the grower and finisher diets; N = total number of production chains
per cluster.

Animal Cluster According to Frequency Percentage

Status of Diet n2
Category 1 Impact [Cluster Number] (n) (%)
dLys deficient low [2] 17 2 11.8
[<0.72 g intermediate [1/4] 15 6 40.0
dLys/MJ NE] high [3] 14 3 21.4
dLys excess low [2] 17 4 25.5
growers
[>0.88 g intermediate [1/4] 15 2 13.3
dLys/MJ NE] high [3] 14 4 28.6
dLys sufficient low [2] 17 11 61.7
[0.72–0.88 g intermediate [1/4] 15 7 64.7
dLys/MJ NE] high [3] 14 7 50.0

153
Sustainability 2018, 10, 3796

Table 11. Cont.

Animal Cluster According to Frequency Percentage

Status of Diet n2
Category 1 Impact [Cluster Number] (n) (%)
dLys deficient low [2] 17 2 11.8
[<0.63 g intermediate [1/4] 16 7 43.8
dLys/MJ NE] high [3] 14 3 21.4
dLys excess low [2] 17 8 47.1
finishers [>0.77 g intermediate [1/4] 16 8 50.0
dLys/MJ NE] high [3] 14 2 14.3
dLys sufficient low [2] 17 7 41.2 ab
[0.63–0.77 g intermediate [1/4] 16 1 6.3 b
dLys/MJ NE] high [3] 14 9 64.3 a
1Parameters that showed significant differences between clusters are printed in bold; 2 classification of diets was
not possible for all PCs; a,b different superscript letters indicate differences between groups (p < 0.05, p-values
adjusted according to Bonferroni correction for triple testing).

4. Discussion

4.1. General Discussion and Comparison with Other Studies

Both hypotheses were confirmed: For all environmental impact categories, variation was greater
within than between systems, with no distinct differences between husbandry systems regarding
their environmental impact. Furthermore, farm characteristics contributing to environmental impact
were identified, and they were mainly related to performance (e.g., piglets weaned per sow and year,
fattening pig feed conversion ratio) and feed characteristics (e.g., percentage of bought-in feed stuff in
fattener diets; see Section 4.2).
The selected classification was chosen according to [1], who found that specific characteristics
(e.g., farm size, breeds, live-weights at slaughtering, etc.) of organic farms suggest this differentiation
into the three husbandry systems. It may be used to inform the organic sector regarding the
strengths and weaknesses of these three widely used systems’ variants, and the results may serve
as a basis for system-specific mitigation strategies. The large range of results indicates potential for
improvement within all three systems. Cluster analysis was used to investigate further classification.
It was interesting to find high, medium, and low impact clusters independently from husbandry
systems, but with characteristics regarding feeding and performance, which are mainly affected by
management decisions.
Comparing different LCA studies should always be done with caution due to differences in
underlying methodology, assumptions, and chosen system boundaries [45]. The present study
addressed, for the first time, the environmental impact of different organic pig husbandry systems
based on data obtained from 64 individual farrow-to-finish production chains across several European
countries. In accordance with [9], there was a high variation in environmental impact among farms in
the present study, indicating that individual farm characteristics highly influenced the outcome.
Other authors report comparable GWP, but rather different AP and EP (Table 12). A possible
reason is that the GWP originating from the main emission source feedstuffs does not differ widely,
except for those loaded with high emissions from land use change. However, in organic systems,
comparably low emissions occur from land use change. Contrarily, emission factors regarding AP and
EP show a higher variation between animals kept indoors or outdoors. Additionally, methodological
differences between studies (e.g., system boundaries, emission factors, type of allocation) could have
contributed to the great variation.
In general, most of our results are within the ranges reported in the literature, e.g., as provided in
a review of six comparable LCA studies of pork products [4] (Table 12). The authors also found a large
variation, especially regarding acidification and eutrophication potential.

154
Sustainability 2018, 10, 3796

Our results are particularly comparable to results reported by [15], who used a similar
methodology and system boundaries for an evaluation of 15 pig farming systems from five European
countries. For each pig farming system, data from five to 10 farms were obtained from surveys,
and systems were categorized into conventional, adapted conventional, traditional, and organic. Feed
production contributed less to EP in organic systems than in the others [15]. In the present study,
the results regarding EP (medians ranging from 20.1 to 28.7 g PO4 -eq per kg live weight) exceed the
values for organic farms found by [15]; 16 g PO4 -eq), and are in the range reported for conventional
systems. The higher EP in the present study may, on the one hand, be due to a poorer median feed
conversion ratio in IN, POUT, and OUT than found by [15]. On the other hand, due to the assumption
of a 5% PO4 -surplus over yield-related plant requirements, our methodological approach might have
resulted in higher PO4 -emission estimates from feed production.
Regarding AP, [15] found higher medians for organic systems than for POUT and OUT in the
present study. The even higher median AP found in IN compared to [15] may be attributed to higher
emissions from manure management (storage and spreading) as well as from feed, which resulted
mainly from a poorer feed conversion ratio in fatteners in the present study compared to [15].

4.2. Factors Influencing the Environmental Impacts

In terms of the relative impact of feed on GWP, AP, and EP, results presented herein agree with
those of other LCA studies [10,22,33,46,47]. Dolman et al. [9] calculated correlations between farm
characteristics and environmental impact: All environmental indicators correlated positively with
feed intake and dietary composition. Likewise, and in accordance with [22], who identified the feed
conversion ratio in fatteners as the parameter with the greatest influence on LCA outcomes, in the
present study, the feed conversion ratio was significantly lower for fatteners in the low impact cluster.
The percentage of bought-in feed for fattener diets (%) was weakly negatively correlated with AP. This
might indicate that these feeds either were loaded with relatively low AP or the feeds contributed to a
better balanced diet and hence an improved feed conversion.
Regarding the relative contribution (%) of feedstuff categories to the environmental impact
indicators, significant correlations were only found for EP. The proportion of high-protein by-products
and minerals negatively correlated with EP, while the proportion of cereal grains was positively
correlated. This might indicate that high-protein by-products and minerals contribute to a better
balanced diet. Furthermore, for fed by-products, a relatively low proportion of impacts from crop
production and processing is allocated to the co-product feed (e.g., molasses or oil cakes), and a rather
high share to the main product, e.g., sugar or oil.
The average fattener carcass weight (kg) was positively correlated with AP and EP, as during
the fattening stage a large proportion of emissions arise. Towards the end of the fattening period the
amount of feed needed for 1 kg of weight gain increases in comparison to earlier growing stages [42].
Furthermore, reproductive performance, especially the number of piglets born alive per litter,
has been described as an important influencing factor [23,48]. However, as for all associations found
in the present study, only weak correlations regarding sow fertility and the environmental impacts
were found. The number of total born (still and live born) piglets per litter negatively correlated
with EP. However, the correlation coefficient again indicated only a weak relationship, therefore,
the results do not allow for strong conclusions. Emissions originating from the sows are allocated to
their offspring, and, therefore, higher litter sizes may be regarded as beneficial if all piglets survive and
grow adequately. However, in light of the effect of litter size on piglet mortality [20], the focus should
be on an adequate litter size, with robust and viable piglets. This suggestion fits to the number of
piglets weaned per sow and year being negatively associated with all environmental impact indicators,
which may indicate that farms with good management and productivity are at an advantage.

155
Sustainability 2018, 10, 3796

Table 12. Greenhouse gas emissions (GWP, kg CO2 -eq/FU), acidification potential (AP, g SO2 -eq/FU),
and eutrophication potential (EP, g PO4 -eq/FU) from selected LCA studies on pig production (FU =
Functional unit).

Source System/Study Case FU GWP AP EP

present results IN (indoor) kg live weight 2.2 61.9 21.6
present results POUT (partly outdoor) kg live weight 2.2 51.9 20.1
present results OUT (outdoor) kg live weight 2.2 55.4 28.7
literature review: range across different
[4] kg pork 3.9–10 43–741 up to 20
conventional systems
[49] organic (outdoors) kg live weight 4.0 92.8 4.1
range across conventional, adapted
[15] kg live weight 2.2–3.4 44-57 16–34
conventional, traditional, organic
[15] organic kg live weight 2.4 57 16
[24] 1,2 conventional, base scenario kg live weight 2.4 44.8 16.1
[10] good agricultural practice kg live weight 2.3 21 44
[10] ‘Label Rouge’ kg live weight 3.5 23 17
1 Results were recalculated to the functional unit of 1 kg of live weight by using the carcass yield mentioned in the
studies; 2 recalculated excluding the slaughter process.

Two farm characteristics describing the size of the pig units (number of slaughtered pigs, livestock
units per PC) negatively correlated with AP and EP, with larger PCs having lower AP and EP.
The current number of sows per PC was also weakly negatively correlated with AP, in line with
the results for other farm size-related characteristics. These results may indicate that larger farms who
are more efficient in managing their pigs, eventually connected with better trained farm staff. Similarly,
negative correlations were found between the average number of fattening pigs and environmental
impact indicators in [9], but this relationship is not considered as causal and may have been related to
potentially better management in larger farms.

4.3. Limitations of the Method and Uncertainties

The present study used primary data from a non-representative sample of farms instead of
modelled data based on assumptions. Therefore, sensitivity analyses, which are used for specific
scenarios, were not applied here. Besides the influence of the PC-specific characteristics, LCA results
depend on underlying methodological assumptions (e.g., emission factors for different floor types,
allocation approach [49]). The degree of uncertainty for estimates revealed from these assumptions
might vary between PCs, and estimates may therefore not be fully appropriate for the diverse
husbandry systems in organic pig farming. A Monte Carlo analysis for the calculation of uncertainties
of primary data as well as emission factors, describing the uncertainty areas of GWP, AP, and EP
results, was not applied in the present study. In future studies on organic pig production, an analysis
of the uncertainties with data from a representative sample of farms should be implemented. In
addition, expanded system boundaries (including, for instance, the impacts of infrastructure) should
be considered in future studies.
In case of emissions from feed production, uncertainty also arises from the fact that all countries’
estimates were based on data for organic feed production in Austria. This approach was considered as
the best option, as comprehensive region-specific data for the production of organic feedstuffs is not
available and calculations of these would have been beyond the project resources.
Furthermore, farm-specific primary data, such as the feed conversion ratio, may be a source of
uncertainty. The calculation of the feed conversion ratio is based on feed use (kg feed fed per day) as
reported by the farmers; losses of feed, occurring especially outdoors, were probably not taken into
consideration by some farmers. Therefore, the calculated feed conversion ratio might be higher (i.e.,
poorer) than the true feed conversion ratio. However, in terms of environmental impact, the amount of
feed should include feed losses.

156
Sustainability 2018, 10, 3796

These limitations offer possible improvements for future studies. As the limitations concern all
husbandry systems, they are not expected to affect the analysis of differences between husbandry
systems. Furthermore, LCA takes numerous aspects into account; if weaknesses concern single aspects,
this does not reduce the meaningfulness of the calculation. Finally, it must be mentioned that, despite
these limitations, the data available for the present PC-specific cradle-to-farm gate LCA with a high
number of organic pig farms included and taking different husbandry systems into account are unique.

5. Conclusions
Regarding environmental impact, a substantial variation was found between individual PCs. The
ranking of the husbandry systems was not consistent regarding environmental impact; whereas the
(median) GWP was similar in all systems; POUT had less AP than IN, and less EP than OUT.
The huge variation among PCs indicates that LCAs based on mean values of model scenarios
will not necessarily be representative for individual farms, which may be subsumed in the modelled
scenario. This reflects the importance of farm specific cradle-to-farm-gate assessments, rather than
generalized scenarios for identifying the extent and the main sources of environmental impact in the
different husbandry systems (IN, POUT, OUT).
In all husbandry systems, PCs with low environmental impacts were found, indicating that IN
and POUT as well as OUT may be managed in an environmentally friendly way. However, a lack of
consistent differences between husbandry systems, as well as results from cluster analysis, indicate that
factors other than the husbandry systems affect the environmental impact of organic pig production.
Feeds generally constitute an important source for environmental impact, with the feed conversion
ratio of fattening pigs being particularly important. Based on cluster analysis, an appropriate dietary
digestible lysine content as well as buying in feedstuffs for supplementation of protein or minerals
appears to be beneficial for a low environmental impact.
Furthermore, manure management (storage and spreading) was identified as a main source of
emissions. Measures, such as covering slurry tanks and direct application of manure to the soil, offer
mitigation options.
The results indicate that an overall good farm management and adequate productivity reduces
the environmental impacts, and hence optimization of management should be the focus irrespective of
the production system.

Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/10/3796/s1,

Equation S1: P-losses into water bodies, Table S1: Emission factors for NH3 , N2 O, N2 and NO3 in outdoor
paddocks, Table S2: Emission factors for housing and manure management systems depending on floor type and
manure type, litter quality, storage period, spreading according to Rigolot et al. [29], Table S3: Characteristics of the
animal production stages by system, Table S4: Characteristics of dietary nutrient content and feed consumption
by system. The values reflect an average dietary content over all diets fed to the animal group. FCR = Feed
conversion rate, n = Number of production chains, Table S5: Percentages of floor type for lactating and pregnant
sows, weaners and fattening pigs kept in the systems indoor (IN) and partly outdoor (POUT), Table S6: Type and
frequency of manure treatment by system, Table S7: Cluster characteristics regarding number of sows on PC at
farm visit, average number of slaughtered fattening pigs/year and number of livestock units (LSU).
Author Contributions: G.R. provided a draft manuscript, which was revised and edited by S.H., S.E., C.W. and
C.L., G.B., J.Y.D., W.Z. additionally reviewed advanced versions of the manuscript. All authors approved the final
version of the manuscript. G.R., D.B., R.B., B.F. and A.P. collected data. G.R., S.H., G.B., R.B., J.Y.D., M.M. and
W.Z. developed the methodological approach and conducted the analysis; J.Y.D. and S.H. provided the software.
Conceptualization and funding acquisition of the project included D.B., S.D., J.Y.D., S.E., B.F., M.M., A.P. and C.L.
Funding: This research was funded by the FP7 ERA-Net, CORE Organic II project “ProPIG”, i.e. the national
CORE Organic II funding agencies of Austria, Switzerland, United Kingdom, Italy, France, Denmark, Germany,
Czech Republic.
Acknowledgments: The authors would like to thank all involved farmers and the ProPIG partners Tine Rousing,
University of Aarhus in Denmark and Gudrun Illmann, Czech University of Life Sciences Prague.
Conflicts of Interest: The authors declare no conflict of interest.

157
Sustainability 2018, 10, 3796

References
1. Früh, B.; Bochicchio, D.; Edwards, S.; Hegelund, L.; Leeb, C.; Sundrum, A.; Werne, S.; Wiberg, S.; Prunier, A.
Description of organic pig production in Europe. Org. Agric. 2014, 4, 83–92. [CrossRef]
2. Lernoud, J.; Willer, H. Current statistics on organic agriculture worldwide: Organic area, producers,
markets and selected crops. In The World of Organic Agriculture. Statistics and Emerging Trends 2015;
Willer, H., Lernoud, J., Eds.; IFOAM: Bonn, Germany; FiBL: Frick, Switzerland, 2015; pp. 32–116. ISBN
978-3-03736-271-6.
3. Goodland, R. Livestock and Climate Change: What if the Key Actors in Climate Change Are... Cows, Pigs and
Chicken? Worldwatch Institute: Washington, DC, USA, 2009.
4. De Vries, M.; de Boer, I.J.M. Comparing environmental impacts for livestock products: A review of life cycle
assessments. Livest. Sci. 2010, 128, 1–11. [CrossRef]
5. Gerber, P.J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling
Climate Change through Livestock—A Global Assessment of Emissions and Mitigation Opportunities; Food and
Agriculture Organization of the United Nations: Rome, Italy, 2013.
6. Jacques, S. Science and animal welfare in France and European Union: Rules, constraints, achievements.
Meat Sci. 2014, 98, 484–489. [CrossRef] [PubMed]
7. FAO. SAFA Sustainability Assessment of Food and Agriculture Systems Guidelines Version 3.0; Food and
Agriculture Organization of the United Nations: Rome, Italy, 2014.
8. Guinée, J.B.; Gorrée, M.; Heijungs, R.; Huppes, G.; Kleijn, R.; Koning, A.; de Oers, L.; van Wegener
Sleeswijk, A.; Suh, S.; Udo de Haes, H.A.; et al. Handbook on Life Cycle Assessment. Operational Guide to the ISO
Standards; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2002.
9. Dolman, M.A.; Vrolijk, H.C.J.; de Boer, I.J.M. Exploring variation in economic, environmental and societal
performance among Dutch fattening pig farms. Livest. Sci. 2012, 149, 143–154. [CrossRef]
10. Basset-Mens, C.; van der Werf, H.M.G. Scenario-based environmental assessment of farming systems:
The case of pig production in France. Agric. Ecosyst. Environ. 2005, 105, 127–144. [CrossRef]
11. Halberg, N.; Hermansen, J.E.; Kristensen, I.S.; Eriksen, J.; Tvedegaard, N.; Petersen, B.M. Impact of organic
pig production systems on CO2 emission, C sequestration and nitrate pollution. Agron. Sustain. Dev. 2010,
30, 721–731. [CrossRef]
12. Olea, R.; Guy, J.; Edge, H.; Stockdale, E.A.; Edwards, S.A. Pigmeat supply chain: Life Cycle Analysis of
contrasting pig farming scenarios. Asp. Appl. Biol. 2009, 95, 91–96.
13. Williams, A.G.; Audsley, E.; Sandars, D.L. Determining the Environmental Burdens and Resource Use in the
Production of Agricultural and Horticultural Commodities; Main Report. Defra Research Project IS0205; Cranfield
University and Defra: Bedford, UK, 2006.
14. Jakobsen, M.; Preda, T.; Kongsted, A.; Hermansen, J. Increased Foraging in Outdoor Organic Pig
Production—Modeling Environmental Consequences. Foods 2015, 4, 622–644. [CrossRef] [PubMed]
15. Dourmad, J.Y.; Ryschawy, J.; Trousson, T.; Bonneau, M.; Gonzàlez, J.; Houwers, H.W.J.; Hviid, M.; Zimmer, C.;
Nguyen, T.L.T.; Morgensen, L. Evaluating environmental impacts of contrasting pig farming systems with
life cycle assessment. Animal 2014, 8, 2027–2037. [CrossRef] [PubMed]
16. IFOAM. The IFOAM Norms for Organic Production and Processing Version 2014; IFOAM: Bonn, Germany, 2014;
ISBN 978-3-944372-10-5.
17. Algers, B.; Blokhuis, H.J.; Bøtner, A.; Broom, D.M.; Costa, P.; Domingo, M.; Greiner, M.; Hartung, J.;
Koenen, F.; Müller-Graf, C.; et al. Scientific opinion of the Panel on Animal Health and Welfare on a request
from the European Commission on species-specific welfare aspects of the main systems of stunning and
killing of farmed carp. EFSA J. 2009, 1013. [CrossRef]
18. The European Parliament and the Council of the European Union. Regulation (EU) 2018/848 of the European
Parliament and of the Council of 30 May 2018 on Organic Production and Labelling of Organic Products; The
European Parliament and the Council of the European Union: Brussels, Belgium, 2018.
19. Edwards, S.A.; Prunier, A.; Bonde, M.; Stockdale, E.A. Special issue—Organic pig production in
Europe—Animal health, welfare and production challenges. Org. Agric. 2014, 4, 79–81. [CrossRef]
20. Prunier, A.; Dippel, S.; Bochicchio, D.; Edwards, S.; Leeb, C.; Lindgren, K.; Sundrum, A.; Dietze, K.; Bonde, M.
Characteristics of organic pig farms in selected European countries and their possible influence on litter size
and piglet mortality. Org. Agric. 2014, 4, 163–173. [CrossRef]

158
Sustainability 2018, 10, 3796

21. Eriksen, J.; Hermansen, J.E.; Strudsholm, K.; Kristensen, K. Potential loss of nutrients from different rearing
strategies for fattening pigs on pasture. Soil Use Manag. 2006, 22, 256–266. [CrossRef]
22. Reckmann, K.; Krieter, J. Environmental impacts of the pork supply chain with regard to farm performance.
J. Agric. Sci. 2015, 153, 411–421. [CrossRef]
23. Garcia-Launay, F.; van der Werf, H.M.G.; Nguyen, T.T.H.; Le Tutour, L.; Dourmad, J.Y. Evaluation of the
environmental implications of the incorporation of feed-use amino acids in pig production using Life Cycle
Assessment. Livest. Sci. 2014, 161, 158–175. [CrossRef]
24. Nguyen, T.L.T.; Hermansen, J.E.; Mogensen, L. Fossil energy and GHG saving potentials of pig farming in
the EU. Energy Policy 2010, 38, 2561–2571. [CrossRef]
25. The British Standards Institution. Publicly Available Specification. PAS 2050: 2011 Specification for the Assessment
of the Life Cycle Greenhouse Gas Emissions of Goods and Services; British Standards Institution: London, UK, 2011.
26. Jespersen, L.M.; Baggesen, D.L.; Fog, E.; Halsnæs, K.; Hermansen, J.E.; Andreasen, L.; Strandberg, B.;
Sørensen, J.T.; Halberg, N. Contribution of organic farming to public goods in Denmark. Org. Agric. 2017, 7,
243–266. [CrossRef]
27. Kool, A.; Blonk, H.; Ponsioen, T.; Sukkel, W.; Vermeer, H.M.; De Vries, J.W.; Hoste, R. Carbon Footprints of
Conventional and Organic Pork: Assessment of Typical Production Systems in the Netherlands, Denmark, England
and Germany; Wageingen UR: Wageningen, The Netherlands, 2009.
28. IPCC. Guidelines for National Greenhouse Gas Inventories; Eggleston Buendia, L., Miwa, K., Ngara, T.,
Tanabe, K.S., Eds.; IPCC: Geneva, Switzerland, 2006.
29. Rigolot, C.; Espagnol, S.; Pomar, C.; Dourmad, J.Y. Modelling of manure production by pigs and NH3 , N2 O
and CH4 emissions. Part I: Animal excretion and enteric CH4 , effect of feeding and performance. Animal
2010, 4, 1401–1412. [CrossRef] [PubMed]
30. Wenzel, H.; Hausschild, M.; Alting, L. Environmental Assessment of Products: Methodology, Tools and Case
Studies in Product Development; Chapman & Hall: London, UK, 1997; Volume 1.
31. Nemecek, T.; Kägi, T. Life Cyce Inventories of Swiss and European Agricultural Production Systems; Final Report
Ecoinvent Report v2.0., No. 15; Agroscope Reckenholz-Taenikon: Zürich and Dübendorf, Switzerland, 2007.
32. Brandhofer, R. Umweltwirkungen Biologischer Schweinehaltung: Vergleich Zweier Haltungssysteme auf
Basis des Treibhausgas-Potenzials Sowie Einer Stickstoff und Phosphorbilanz. Master’s Thesis, University of
Natural Resources and Life Sciences, Vienna, Austria, 2014.
33. Basset-Mens, C.; van der Werf, H.M.G.; Robin, P.; Morvan, T.; Hassouna, M.; Paillat, J.M.; Vertès, F. Methods
and data for the environmental inventory of contrasting pig production systems. J. Clean. Prod. 2007, 15,
1395–1405. [CrossRef]
34. Dourmad, J.Y.; Physiology of Adaptation, Animal Nutrition and Health, INRA, Saint-Gilles, France. Personal
communication, 2013.
35. Hörtenhuber, S.; Lindenthal, T.; Amon, B.; Markut, T.; Kirner, L.; Zollitsch, W. Greenhouse gas emissions
from selected Austrian dairy production systems—Model calculations considering the effects of land use
change. Renew. Agric. Food Syst. 2010, 25, 316–329. [CrossRef]
36. Hörtenhuber, S.J.; Lindenthal, T.; Zollitsch, W. Reduction of greenhouse gas emissions from feed supply
chains by utilizing regionally produced protein sources: The case of Austrian dairy production. J. Sci.
Food Agric. 2011, 91, 1118–1127. [CrossRef] [PubMed]
37. Kolbe, H. Wasserbelastung in Abhängigkeit von der Landnutzung. Available online: http://orgprints.org/
801/ (accessed on 19 October 2018).
38. Samuel-Fitwi, B.; Meyer, S.; Reckmann, K.; Schroeder, J.P.; Schulz, C. Aspiring for environmentally conscious
aquafeed: Comparative LCA of aquafeed manufacturing using different protein sources. J. Clean. Prod. 2013,
52, 225–233. [CrossRef]
39. LCA Food database. Aalborg University and 2.-0 LCAconsultants. 2007. Available online: http://www.
lcafood.dk/ (accessed on 19 Oct 2018).
40. Leeb, C.; Bernardi, F.; Winckler, C. Einführung und Monitoring von BetriebsEntwicklungsPlänen (BEP)
Tiergesundheit und Wohlbefinden in Österreichischen Bioschweinebetrieben; Institut für Nutztierwissenschaften:
Vienna, Austria, 2010.
41. Bayern, L. Schweinefütterung am Ökobetrieb II—Fütterungsversuche, Fütterungsempfehlungen; LfL Bayern: Poing,
Germany, 2011.

159
Sustainability 2018, 10, 3796

42. Kirchgessner, M.; Roth, F.X.; Schwarz, F.J.; Stangl, G. Tierernährung. Leitfaden für Studium, Beratung und Praxis,
13th ed.; DLG Verlag: Frankfurt, Germany, 2011.
43. EvaPig® . A Calculator of Energy, Amino Acid and Phosphorus Values of Ingredients and Diets for Growing
and Adult Pigs. Available online: http://www.evapig.com (accessed on 19 October 2018).
44. Alibert, L. Besoins Alimentaires des Animaux en Fonction du Stade Physiologique. Available online:
http://www.itab.asso.fr/downloads/porc-bio/cahier_porc_0.pdf (accessed on 10 Dec 2014).
45. Lammers, P.J. Life-cycle assessment of farrow-to-finish pig production systems: A review. CAB Rev. Perspect.
Agric. Vet. Sci. Nutr. Nat. Resour. 2011, 6, 1–8. [CrossRef]
46. Pelletier, N.; Lammers, P.; Stender, D.; Pirog, R. Life cycle assessment of high- and low-profitability
commodity and deep-bedded niche swine production systems in the Upper Midwestern United States.
Agric. Syst. 2010, 103, 599–608. [CrossRef]
47. Alig, M.; Grandl, F.; Mieleitner, J.; Nemecek, T.; Gaillard, G. Life Cycle Assessment of Beef, Pork and Poultry;
Executive Summary; Reckenholz-Tänikon: Zürich, Switzerland, 2012.
48. Dalgaard, R.; Halberg, N.; Hermansen, J.E. Danish Pork Production—An Environmental Assessment; University
of Aarhus: Tjele, Denmark, 2007; Volume 82.
49. Mackenzie, S.G.; Leinonen, I.; Ferguson, N.; Kyriazakis, I. Accounting for uncertainty in the quantification of
the environmental impacts of Canadian pig farming systems Supplementary Material. J. Anim. Sci. 2015, 93,
3130–3143. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

160
 sustainability

Article
Effects of Alternative Uses of Distillery By-Products
on the Greenhouse Gas Emissions of Scottish Malt
Whisky Production: A System Expansion Approach
Ilkka Leinonen 1, *, Michael MacLeod 1 and Julian Bell 2
1 Land Economy, Environment and Society Research Group, Scotland’s Rural College (SRUC),
Peter Wilson Building, Kings Buildings, West Mains Road, Edinburgh EH9 3JG, UK;
[email protected]
2 Rural Business Unit, SAC Consulting, 2 Technopole, Bush Estate, Penicuik, Midlothian EH26 0PJ, UK;
[email protected]
* Correspondence: [email protected]; Tel.: +44-131-5354044

Received: 6 April 2018; Accepted: 4 May 2018; Published: 8 May 2018

Abstract: Agricultural by-products are an important component of livestock feed. In Scotland,

distillery by-products are protein rich and traditionally cost competitive feed ingredients in cattle
production. However, during recent years, distilleries in the UK (including Scotch whisky producers)
have started to use the by-products also as a source of renewable energy, in order to reduce the carbon
footprint of alcohol production. In this study, a systems-based material and energy flow analysis
was performed to calculate the life-cycle greenhouse gas (GHG) emissions of whisky production
for two scenarios where distillery by-products were used either (1) as beef cattle feed to replace
other protein sources (namely soya bean meal and rapeseed meal); or (2) as anaerobic digester (AD)
feedstock in order to generate renewable energy (heat and electricity). System expansion was used to
quantitatively handle the by-products in the analysis. The results show that considerable reductions
in GHG emissions could be achieved by either replacing feed crops with by-products or by using the
by-products in AD plants to generate bio-energy. The biggest reductions in the GHG emissions were
achieved when by-products were used to replace soya meal in animal feed. However, the results are
highly sensitive to methodological choices, including the accounting method of the land use change
emissions arising from soya production.

Keywords: agricultural by-products; whisky production; cattle; beef; livestock feed; renewable
energy; greenhouse gas emissions

1. Introduction
Various agricultural by-products (i.e., products originating from food and drink production but
not normally used for human consumption) are widely used as part of livestock feed. They can form
an important source of protein and metabolizable energy needed for animal production [1–4] and are
currently used in production of a wide variety of livestock species [5]. For example, brewery, spirit
distillery and bio-ethanol production by-products, such as brewers’ grains, usually made from barley,
wheat, maize or rice, can form a significant part of the animal diet especially in ruminant production.
These products are generally favoured due to their high protein and fibre content [6–10] and inclusion
of them in ruminant feed has been found to have positive effects on the animal performance [11,12].
Brewers’ grains, or further processed distillery by-product “distillers dark grains with solubles” or
“dried distillers grains with solubles” (DDGS), can be also used in non-ruminant production, for
example, as part of pig feed [13–17]. According to recent studies, relative high proportions of DDGS
can be applied in pig diets while still maintaining acceptable level of growth performance [15,16,18].

Sustainability 2018, 10, 1473; doi:10.3390/su10051473 161 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 1473

Further application of brewery and distillery by-products such as DDGS and yeast products can also
be found in chicken industry [19–23], or even in fish production [24,25]. However, high variability in
the nutritional value of these by-products, depending for example on the variety of the cereal, harvest
time and the malting and mashing processes [10,26,27] may limit their use in non-ruminant livestock
production where the content of certain nutrients, especially the balance of essential amino acids,
can have major impact on animal performance [28]. Despite such limitations, brewery and distillery
by-products can be potentially seen as a partial replacement of soya as a protein source in livestock
production [20,29,30]. Reducing the dependency on soya is an increasing trend in livestock systems
due to environmental concerns related to its production. The cultivation of this crop is generally
associated with recent land use changes, causing greenhouse gas emissions from deforestation and
conversion of other land uses to arable production, resulting in loss of carbon previously stored in
soil and biomass [31]. Other environmental issues associated with soya production include the loss of
biodiversity and freshwater and groundwater contamination [32,33].
The availability and usability of agricultural by-products or co-products can vary strongly
depending on the location of production and this can also affect the distribution and profitability of
livestock industries. In agricultural production in Scotland, barley is by far the most important arable
crop species, in terms of area of cultivation, the total mass of grain production and the amount of crop
protein produced [34]. The barley grown in Scotland is used either directly for animal feed, or as a raw
material of alcohol (including whisky) production. The whisky distillation process utilizes only the
carbohydrates of the barley grains, so therefore the use of the remaining compounds (including protein)
in livestock production has been seen as a useful way to fully utilize this important crop. As a result,
the main by-products of Scottish malt whisky production, namely “draff” (unprocessed by-product
of the mashing process), “pot ale” (liquid by-product of distillation) and “distillers dark grains with
solubles” (DDGS, dried and pelletized product made of draff and pot ale) are widely used as protein
rich and low-cost ingredients of livestock feed, particularly in beef and dairy cattle production. In 2012,
it was estimated that a total of 346,000 t (on a dried product basis) of distillery by-products from the
whisky industry in Scotland were potentially available for use in animal feed [35]. About 60% of this
amount was consumed in Scotland. Therefore, in this specific region, whisky industry and the feed that
it provides for livestock can be considered as a significant part of the beef and dairy production chains.
Distillery by-products used as feed have been considered to have low environmental impacts
and especially low embedded greenhouse gas (GHG) emissions, compared to alternative protein
sources such as rapeseed meal and imported soya [35,36]. One of the reasons for this finding is that in
agricultural life cycle assessment (LCA) studies, economic allocation of the environmental burdens is
generally applied to distribute the burdens between various co-products originating from the same
production process [37–39]. In this specific method, the burdens are allocated to different co-products
proportionally to their economic value [3,36]. Therefore, due to a relatively low price of the distillery
by-products such as draff, the produced alcohol is considered to be the main product with the highest
share of the environmental burdens and only a small proportion of the overall environmental impacts
associated with whisky production is allocated to by-products [35].
In addition to the traditional use of distillery by-products as livestock feed, distilleries in Scotland
(and other alcohol producers in the UK) have during recent years started to use these products as
a source of renewable energy. This development is partly motivated by the government subsidies
for such energy sources due to their low embedded GHG emissions. Furthermore, the reduction
of the use of fossil fuels in the production process can also provide a greener image for the whisky
industry through reducing its carbon footprint [40]. A recent trend in this area has been to increase the
use of by-products as a feedstock of anaerobic digestion and utilize the produced biogas to generate
electricity and heat that can be directly used in the distillation process. This strategy is expected to have
multiple benefits in terms of reduction of GHG emission. For example, in addition to the renewable
energy generated in digestion, the digestate (material remaining after the anaerobic digestion process)

162
Sustainability 2018, 10, 1473

contains nutrients that can be utilized by crops and therefore can replace the use of synthetic fertilisers
and reduce the greenhouse gas emissions related to production of the fertilisers [41,42].
The proposed alternative use of distillery by-products has raised some concerns amongst livestock
farmers in Scotland and elsewhere in the UK [43]. As the use as renewable energy increases, the farmers
are getting worried about the future availability and cost of by-products as animal feed. However, it
should be noted that also the feed use of these by-products can be expected to have beneficial effects
on greenhouse gas emissions due to reduction of the use of carbon-intensive feed ingredients. For this
reason, a systematic comparison of GHG emissions associated with alternative uses of by-products is
needed to quantify these possible effects.
The aim of this study was to carry out a systems-based analysis of the material and energy flows
within the whisky production chain, in order to quantitatively analyse the processes associated with
distillery by-products and assess the life-cycle greenhouse gas emissions arising from the entire whisky
production chain, including the end use of by-products. Instead of applying an economic allocation
approach for the outputs of the distillery processes, we selected to use a system expansion method for
the by-products, specified as “expanding the product system to include the additional functions related
to the co-products” in the ISO [44] LCA standards. Those standards also prefer the system expansion
approach over any allocation methods and suggest that allocation between co-products should be
avoided when possible. The system expansion approach makes it possible to directly compare the
changes in greenhouse gas emissions when using the by-products for alternative purposes (livestock
feed, bioenergy generation) and replacing alternative commodities (protein crops grown for cattle
feed, fossil fuels used in distillation process, synthetic fertilisers used in crop production). As an
outcome, the greenhouse gas emissions can be calculated for a unit of produced alcohol while taking
into account both the burdens and benefits achieved through the end use of the by-products.

2. Materials and Methods

A systems-based material flow analysis linking the Scottish malt whisky production and the
end use of its by-products either in a cattle production system or in energy generation processes
was carried out (Figure 1) to quantify the life-cycle GHG emissions arising from whisky production.
The analysis applied a system expansion approach, that is, whisky was considered as the main
product of distilleries, the by-products of the process were used to replace alternative commodities
and the changes in greenhouse gas emissions as a result of this replacement were accounted for
when quantifying the overall emissions of whisky production. In order to achieve this, the whisky
production system was linked to other systems affected by the by-product use, namely beef cattle
production system, crop production system and energy generation system (see detailed system diagram
in Supplementary Materials). The changes in the material and energy flows within these connected
systems were analysed and the associated GHG emissions quantified as detailed below. This approach
was used to calculate the greenhouse gas emissions for two baseline scenarios: Scenario 1: distillery
by-products were used as cattle feed to replace either soya bean meal or rapeseed meal as a protein
source (while maintaining the nutritional quality of the feed) and Scenario 2: distillery by-products
were used as anaerobic digester (AD) feedstock in order to generate renewable energy (heat and
electricity). For both of these scenarios, the functional unit was 1 litre of pure alcohol (LPA) and the
system boundary was from cradle to the end of the distillation process. However, instead of the whisky
production chain itself (which remained the same in both baseline scenarios), the main focus of this
study was in the effects of alternative uses of the by-products on GHG emissions in other, connected
systems, analysed through the system expansion approach.

163
Sustainability 2018, 10, 1473

Figure 1. A simplified diagram of the production systems analysed in this study and processes affecting
the greenhouse gas (GHG) emissions. The rectangles indicate inputs or outputs and the ovals indicate
processes. The objects with broken lines indicate replaced products or processes partly affected by
the replacement.

The greenhouse gas emissions associated with whisky production (including production,
processing and transport the raw materials but excluding the by-product processing and their end use)
were quantified based on data from an earlier study [35] and the changes of these emissions, as affected
by the alternative uses of the by-products, were included in the calculations. Details of the data and the
calculated GHG emissions associated with different processes within the whisky production chain can
be found in the Supplementary Materials. Following this analysis, the processing and end use of the
by-products was analysed in different scenarios, the changes in the material and energy flows within
connected systems were quantified and the resulting increases or reductions of GHG emissions were
included in the total emissions of the whisky production chain. For this analysis, the quantities of the
primary by-products produced per one litre of pure alcohol were obtained from the calculations by
Bell et al. [35] and were estimated to be 0.56 kg DM of draff and 0.36 kg DM of pot ale. In all the systems
included in the calculations, the changes in the emissions of carbon dioxide (CO2 ), methane (CH4 )
and nitrous oxide (N2 O) were quantified and the overall greenhouse gas emissions were expressed in
terms of CO2 equivalent: with a 100-year timescale, where 1 kg CH4 and N2 O are equivalent to 25 and
298 kg CO2 respectively [45].

2.1. Scenario 1: Distillery By-Products as Livestock Feed

In this scenario, the amounts of replaced feed ingredients in livestock production were quantified,
together with the resulting changes in GHG emissions associated with feed production, enteric
fermentation, manure management and fertiliser use in crop production. Two alternative by-products
of malt whisky distilleries were used as a protein source in cattle feed, namely draff and DDGS. Draff
was used fresh, without further processing, while DDGS was produced as a combination of draff and
pot ale and additional processing (drying and pelletizing) was needed in its production. The use of
distillery by-products was assumed to replace two alternative protein sources widely used in Scottish

164
Sustainability 2018, 10, 1473

cattle industry, namely soya bean meal and rapeseed meal. As a result, four different options in the
feed use of the by-products were considered separately:

• Scenario 1a: draff is used to replace soya bean meal (and pot ale is disposed)
• Scenario 1b: draff is used to replace rapeseed meal (and pot ale is disposed)
• Scenario 1c: draff and pot ale are used to produce DDGS, which is used to replace soya bean
meal, and
• Scenario 1d: draff and pot ale are used to produce DDGS, which is used to replace rapeseed meal

The amounts of the replaced alternative ingredients in animal feed were quantified based on
a feeding strategy according to which the digestible protein and metabolizable energy contents of
the feed were kept unchanged for all scenarios, although the intakes of the total combustible “gross”
energy and the total (digestible + non-digestible) protein (and therefore also the total nitrogen intake)
could vary between feeding options. Using this approach, also the animal performance was assumed
to remain unchanged (for example, the same amount of meat was always produced per unit of energy
or protein fed into the beef production system) and would therefore have no effect on the greenhouse
gas emissions when compared between the scenarios. Because the protein content of the distillery
by-products is lower than that of the replaced soya meal or rapeseed meal, on dry matter (DM) basis
higher quantities of the by-products were needed, compared to the replaced ingredients. The higher
DM quantity of the by-products brought also additional energy to the feed. Therefore, other changes
in the feed were also needed to achieve equal energy content. This was done in this study by reducing
the inclusion of barley grains (which are a typical source of energy in cattle feed in Scotland) when the
distillery by-products were used in the feed. Linear optimization was used (with the constraints of
equal protein and energy content) to determine the quantities of the replaced ingredients to equal 1 kg
DM of the by-product for both draff and DDGS feeding scenarios.
The nutrient contents of different feed ingredients were based on the Feedipedia [46] database.
Assuming unchanged digestible protein and energy intake, the nutritional data were used to quantify
the differences in the animal intake of dry matter and nutrients when either distillery by-products or
alternative ingredients were used in the feed and this information was used to quantify the changes of
the greenhouse gas emissions arising from the livestock production system (see below).
The greenhouse gas emissions of the production of the replaced feed ingredients (soya bean meal,
rapeseed meal, barley) were calculated using the Scottish Agricultural Emission Model (SAEM) [47],
which is based on the FAO GLEAM livestock model [48,49]. Details of SAEM can be found in the
Supplementary Materials. The emissions related to land use changes (LUC) arising from South
American soya production were also included in the calculations following the FAO [48] approach
and emission factors [47]. However, since there are plenty of uncertainties in the LUC emissions
and differences in the methods for accounting for those in the context of agricultural production
chains, alternative estimates of those emissions were evaluated in the sensitivity analysis (see below).
The other replaced feed crops apart from soya, that is, rapeseed and barley, were assumed to be
originated from “mature” agricultural land in the UK and therefore no LUC emissions were associated
with those feed ingredients [50,51].
The changes in the greenhouse gas emissions arising from enteric fermentation and manure
management, resulting from the changes in the feed composition, were also quantified and taken into
account in the analysis. The calculation of these emissions was based on the intake of nitrogen and
gross energy by the animal, applying the IPCC [45] Tier 2 approach and SAEM [47] emission factors
(Table 1, Supplementary Materials). In this approach, the emissions of CH4 are proportional to the feed
gross energy intake of the animal and the N2 O and NH3 emissions are proportional to the amount of
nitrogen excretion (affected by the protein content of the animal feed intake).

165
Sustainability 2018, 10, 1473

Table 1. Emission factors and other constants used in the life cycle assessment (LCA) model.

Factor Value Source

GHG emissions from rapeseed production, kg CO2 e per kg DM 0.86 [47]
GHG from barley production, kg CO2 e per kg DM 0.325 [47]
LUC emissions from soya meal production, kg CO2 e per kg DM 3.25 [47,48]
Other GHG emissions from soya meal production, kg CO2 e per kg DM 0.83 [47]
GHG emissions from N fertiliser production, kg CO2 e per kg N 6.8 [53]
GHG emissions from P fertiliser production, kg CO2 e per kg P 3.3 [53]
GHG emissions from K fertiliser production, kg CO2 e per kg K 1.0 [53]
GHG emissions from UK grid electricity, kg CO2 e per kWh 0.465 [54]
GHG emissions from heating oil, kg CO2 e per kWh 0.267 [54]
Volatile solids of DM of distillery by-products 91% [55]
CH4 yield, m3 per kg VS 0.385 [55]
Biogas CO2 content 40% [56]
AD/digestate CH4 leakage 3% [56]
Other digestate C losses 10% [57]
Feed/AD feedstock DM carbon content 47.5% [58]
Long-term (20 years) soil C storage of all soil C input 15% [59]
CHP electricity yield of total CH4 energy 36% [56]
CHP heat yield of total CH4 energy 40% [56]
Electricity fed back to AD 12% [56]
Heat fed back to AD 9% [56]
Proportion of net heat utilized 60% [56]
Digestate/manure N fertiliser replacement value 65% [52]
Digestate/manure P fertiliser replacement value 100% [52]
Digestate/manure K fertiliser replacement value 100% [52]
CH4 from enteric fermentation, kg CH4 per MJ GE 0.0012 [45,47]
Direct manure management N2 O emissions, % N2 O-N of total N 0.2% [45,47]
Indirect manure management N2 O emissions, % N2 O-N of total N 0.13% [45,47]
Total manure management N losses: volatilized 12.5% [47]
Total manure management N losses: leached 1.7% [47]

The differences in the contents of main available plant nutrients, namely nitrogen (N), phosphorus
(P) and potassium (K) in the manure, as affected by alternative scenarios, were calculated on the basis
of nutrient intake and subsequent losses (assuming that the nutrient retention in animal body remained
unchanged regardless of the feed ingredients used) and their benefits in reducing the greenhouse
gas emissions by replacing synthetic fertilisers were quantified. The replacement rates of synthetic
fertilisers applied in this study were based on the study by DeVries et al. [52]. The greenhouse gas
emissions from the replaced synthetic fertiliser production were quantified by using the emission
factors of the SAEM beef model [47,53].
Changes in the soil carbon (C) content (carbon sequestration) as a result of manure fertiliser use
were not considered in the baseline calculations. However, the possible effects of changes of the carbon
input to soil are evaluated in the sensitivity analysis (see below).

2.2. Scenario 2: Distillery By-Products as a Source of Renewable Energy

In this scenario, the amounts of replaced commodities were quantified when the by-products were
used as an energy source. These commodities include grid electricity, fossil fuels used for heating and
fertilisers used in crop production. The changes in GHG emissions associated with energy generation,
management of the digestate and production of the fertiliser were then quantified as detailed below.
Two by-products of whisky production, namely draff only (Scenario 2a) and a combination of draff
and pot ale (Scenario 2b), were used as feedstock of anaerobic digestion (AD) to produce biogas.
These scenarios were selected so that in terms of the input material, Scenario 2a was comparable to
the feed use scenarios 1a and 1b (using draff directly as a feed ingredient) and Scenario 2b comparable
to Scenarios 1c and 1d (using draff and pot ale to produce DDGS for feed). Unlike in Scenarios 1c and

166
Sustainability 2018, 10, 1473

1d, no further processing of by-products (needed to produce DDGS) was applied in Scenario 2b, as
such processing would have no value in biogas production.
The produced biogas was assumed to be subsequently used to generate heat needed in mashing,
fermentation and distillation processes and electricity to be fed to electrical grid, using the combined
heat and power (CHP) technology.
The yield of CH4 per kg of DM of distillery by-products was obtained from
Luna-del Risco et al. [55] and the same value was used for both Scenario 2a and 2b (Table 1).
The yields of electricity and heat generated in the CHP process, the proportions of the generated
electricity and heat needed in the AD process and efficiency of the utilization of the net heat were
obtained from an earlier study carried out at SRUC [56]. The heat obtained from the use of the
biogas was assumed to replace part of the use of fuel oil, which is a commonly used fuel in Scottish
malt whisky production as many distilleries are remote and not on the natural gas grid. Finally,
the replacement of the grid electricity (i.e., the electricity fed to the grid minus the electricity used
in the AD process) and the utilizable heat (net heat production minus the heat used in the AD
process) were quantified, the associated greenhouse gas emissions were calculated based on the
UK Department for Business, Energy & Industrial Strategy emission factors [54] and these avoided
emissions were subtracted from the total greenhouse gas emissions of whisky production.
The direct and indirect greenhouse gas emissions arising from the AD and CHP processes and
from the management of the digestate were also quantified and added to the emissions of whisky
production. The methane leakage was based on values from an earlier study carried out at SRUC [56]
and the N2 O and NH3 emissions where based on the nutrient content of the feedstock, obtained from
the Feedipedia [46] database and calculated in a same way as the emissions from manure management.
Similarly, as in the use of the by-products as feed, the fertiliser value of the nutrients obtained
as an output of the AD process was quantified. All phosphorus and potassium of the feedstock were
assumed to remain in the digestate and the nitrogen emissions described above were subtracted from
the total nitrogen content of the digestate. The remaining nutrients could then be expected to replace
synthetic fertilisers. It should be noted that part of the grid electricity is also generated from biomass
(in 2016, this was estimated to be 7.6%, according to Ofgem [60] data) and was therefore assumed to
replace a similar amount of fertiliser per kWh of generated electricity as the AD system considered
here. To avoid double counting, a proportion equal to this share was subtracted from the applicable
organic fertilisers produced in the AD. Similarly, as in Scenario 1, the changes in soil carbon content
were not included in this baseline but they are evaluated in the sensitivity analysis.
A summary of the emission factors and other constants used in the calculations for different
scenarios can be found in Table 1.

2.3. Sensitivity Analysis

2.3.1. LUC Emissions

In the baseline analyses, the emissions arising from the land use changes associated with the
soya production were based on the FAO [48] default calculations methods, resulting in an emission
factor of 3.25 kg CO2 equivalent per kg DM soya bean meal [47]. However, alternative estimates
of this value exist, so two alternatives were used here for comparison. First, recent calculations by
Williams et al. [59] estimated the direct LUC emissions to be 1.46 kg CO2 e per kg DM soya bean meal
(based on weighted average of the origins of soya used in the UK). Second, assuming that the soya
would originate from sustainable sources, (i.e., no LUC associated with its production) and following
the methods of PAS 2050 carbon footprinting guidelines [50,51], the LUC emissions would be zero.

2.3.2. Carbon Sequestration

Although soil carbon content is not normally considered in agricultural LCA, changes in the
ecosystem carbon stock are included in the IPCC [45] guidelines for calculating GHG emissions.

167
Sustainability 2018, 10, 1473

For this reason, alternative calculations were carried out where the changes of soil carbon content
in different scenarios were estimated. First, the amount of carbon in the digestate was determined
based on the carbon content of the AD feedstock [58] and the carbon losses as CO2 and CH4 during
the digestion process. For the animal feed, it was assumed that the dry matter excretion rate is
inversely proportional to the organic matter digestibility, obtained from the Feedipedia [46] database
and a constant carbon content of the excreted organic matter was used in the calculations [58]. Then,
the changes of the carbon input entering soil (in the fertiliser use of digestate or manure) were
quantified in each scenario. Finally, following the method introduced by Williams et al. [59] and
assuming the same decomposition rate of organic matter as in their study, the proportion of the
carbon remaining in the soil within a 20-year time scale (consistent with the IPCC [45] guidelines) was
determined to be 15% of the total addition of carbon to soil. This was then converted to avoided CO2
emissions and subtracted from the greenhouse gas emissions of whisky.

3. Results and Discussion

The potential of the distillery by-products to replace different feed ingredients in either soya meal
based (Scenarios 1a and 1c) or rapeseed meal based (Scenarios 1b and 1c) feed is presented in Table 2.
The results show that using an equal amount of the by-product, generally a bigger amount of rapeseed
meal could be replaced than soya bean meal, due to the lower protein content of the former. It can
be also seen that on the dry matter basis, DDGS is more efficient than draff in replacing alternative
protein sources.

Table 2. The amounts of different feed ingredients in cattle feed replaced by the distillery by-products
(Draff or dried distillers grains with solubles (DDGS)) in different scenarios. The quantities are based
on equal content of metabolizable energy and digestible protein.

By-Product (1 kg DM) Replaced Soya Meal, kg DM Replaced Rapeseed Meal, kg DM Replaced Barley, kg DM
Draff: Scenario 1a 0.28 0.41
Draff: Scenario 1b 0.44 0.32
DDGS: Scenario 1c 0.39 0.54
DDGS: Scenario 1d 0.60 0.42

Replacement of alternative feed ingredients resulted in considerable reductions in greenhouse

gas emissions arising from feed production (Table 3). When comparing different alternative protein
sources (soya and rapeseed), higher reductions could be achieved when soya bean meal was removed
from the feed, due to avoided emissions that would arise from land use changes associated with
soya production.

Table 3. Effects of replacing soya bean meal or rapeseed meal in cattle feed by distillery by-products
(Draff or DDGS) on GHG emissions arising from different sources (kg CO2 equivalent per 1 kg DM of
by-product). Negative signs indicate reduction of emissions and positive signs increase of emissions.

Draff Replacing Draff Replacing DDGS Replacing DDGS Replacing

Source of GHG Emission
Soya (Scenario 1a) Rapeseed (Scenario 1b) Soya (Scenario 1c) Rapeseed (Scenario 1d)
Feed production −1.288 −0.480 −1.773 −0.655
Manure N2 O 0.002 −0.001 0.003 −0.001
CH4 enteric fermentation 0.063 0.049 0.14 0.066
N fertiliser replacement −0.005 0.001 −0.007 0.001
P fertiliser replacement 0.001 −0.005 −0.016 −0.024
K fertiliser replacement 0.009 0.002 0.002 −0.007
Processing (DDGS) 0 0 0.518 0.518
Total −1.219 −0.433 −1.133 −0.101

There were only minor changes in emissions directly related to livestock production, other than
those arising from feed production, when distillery by-products were replaced with alternative feed

168
Sustainability 2018, 10, 1473

ingredients (Table 3). The reason for that is that the inputs (gross energy intake, nutrient intake)
affecting those emissions in the calculations based on IPCC Tier 2 method remained very similar in all
feeding scenarios. This is expected, as the quantities of the feed ingredients consumed by the animals
were specified so that the metabolizable energy intake and the digestible protein intake (affecting N
emissions) remained constant in all scenarios. The differences in those emissions were thus a result of
small differences in the contents of nutrients in the feed and different digestibility of energy and protein
in different feed ingredients. These factors affected the avoided emissions related to the production of
replaced fertilisers but the differences in those emissions were also rather small between the feeding
scenarios with different feed ingredients.
The outputs of the scenario where the distillery by-products were used to generate renewable
energy are presented in Table 4. In addition to the generated electricity and heat (replacing grid
electricity and heating oil used in whisky production), considerable amounts of synthetic fertilisers
could also be replaced when the digestate obtained from the anaerobic digestion would be used as a
fertiliser in crop production.

Table 4. Outputs of use of distillery by-products as a source of renewable energy by applying a

combination of anaerobic digester (AD) and combined heat and power (CHP) (per 1 kg of dry matter
(DM) of the by-product).

Outputs per 1 kg DM by-Product Draff (Scenario 2a) Draff + Pot Ale (Scenario 2b)
Methane, m3 0.351 0.351
Electricity to grid, kWh 1.146 1.146
Utilized heat, kWh (replacing oil) 0.790 0.790
Replaced N as fertiliser, kg 0.018 0.024
Replaced P as fertiliser, kg 0.003 0.009
Replaced K as fertiliser, kg 0.0003 0.009

Since the same conversion factor for methane yield was used for different types of distillery
by-products when used as AD feedstock [55], there were no differences in the amount of energy
generated per unit of DM between the options where draff only or a combination of draff and pot ale
were used in AD. However, there were differences in the amount of fertiliser that could be replaced by
the digestate, depending on the feedstock used. This was due to the high nutrient content of pot ale
and for this reason, the digestate from the combination of draff and pot ale had a higher capacity to
replace fertilisers than the digestate originating from draff only.
The biggest part of the reductions in the greenhouse gas emissions, when distillery by-products
were used as AD feedstock, was associated with the replaced grid electricity (Table 5). However,
considerable reductions were achieved also by using the digestate to replace synthetic fertilisers, most
notably nitrogen fertilisers. Unlike in the Scenario 1, most of the nutrients entering to the AD process
as part of the feedstock could actually be credited to whisky production. In contrast, in the feed use,
the difference in the nutrient output between the by-products and the alternative feed ingredients was
rather small. The reduction of the GHG emissions was also affected by the emissions of methane and
nitrous oxide arising from the digestion process and storage of the digestate (Table 5).

169
Sustainability 2018, 10, 1473

Table 5. Effects of using distillery by-products as a source of renewable energy (by applying a
combination of AD and CHP) on GHG emissions arising from different sources (kg CO2 equivalent per
1 kg DM of by-product). Negative signs indicate reduction of emissions and positive signs increase
of emissions.

Source of GHG Emission Draff (Scenario 2a) Draff + Pot Ale (Scenario 2b)
Electricity replacement −0.549 −0.549
Oil replacement −0.25 −0.25
N fertiliser replacement −0.12 −0.159
P fertiliser replacement −0.011 −0.03
K fertiliser replacement −0.000 −0.009
N2 O emissions 0.051 0.063
CH4 emissions 0.176 0.176
Total −0.703 −0.759

Total GHG emissions per volume unit of produced alcohol were 2.6 kg CO2 when the end use
of the by-products was excluded from the calculations [35]. The changes in these emissions when
the draff obtained from the mashing process was used either as animal feed or as AD feedstock are
presented in Table 6 and Figure 2. It can be seen that the highest overall reductions were achieved
when draff was used to replace soya in animal feed. However, nearly as high reduction could be
achieved when draff was used to generate renewable energy.

Table 6. Effects of the alternative uses of draff on the GHG emissions of Scottish malt whisky production.
The following scenarios are compared: Scenario 1a: draff replacing soya bean meal and barley, Scenario
1b: draff replacing rapeseed meal and barley and Scenario 2a: draff replacing grid electricity and oil.

Amount of Draff Effect on GHG Emissions, kg Final GHG

Produced, kg DM per CO2 e per Litre of Alcohol Emissions per Litre
Litre of Alcohol (Relative Change in Parentheses) of Alcohol, kg CO2 e
Scenario 1a: Replacing soya 0.56 −0.68 (−26%) 1.92
Scenario 1b: Replacing rapeseed 0.56 −0.24 (−9%) 2.36
Scenario 2a: Renewable energy 0.56 −0.39 (−15%) 2.21

When comparing the alternative uses of DDGS (or a combination of draff and pot ale), the patterns
were somewhat different (Table 7, Figure 2). Compared to draff, the combination of draff and pot
ale was able to produce higher reductions in GHG emissions when used either to replace soya in
animal feed, or to generate renewable energy. The reason for this is partly in the larger amount of
the by-product utilised per unit of produced alcohol and also in the high nutrient content of pot ale.
This enabled the combination of draff and pot ale to replace higher amount of alternative protein
sources in animal production, or replace more fertilisers when the digestate is used in crop production.
In contrast, only minimal reductions in the GHG emissions were achieved when DDGS was used to
replace rapeseed meal in animal feed. This is due to the fact that the benefits achieved by reducing
the amount of rapeseed in feed are counteracted by the high energy use of producing DDGS from the
primary by-products draff and pot ale.

170
Sustainability 2018, 10, 1473

Table 7. Effects of the alternative uses of combination of draff and pot ale on the GHG emissions of
Scottish malt whisky production. The following scenarios are compared: Scenario 1c: DDGS replacing
soya bean meal and barley, Scenario 1d: DDGS replacing rapeseed meal and barley and Scenario 2b:
draff + pot ale replacing grid electricity and oil.

Amount of Draff + Pot Effect on GHG Emissions, kg Final GHG

Ale Produced, kg DM CO2 e per Litre of Alcohol Emissions per Litre
per Litre of alcohol (Relative Change in Parentheses) of Alcohol, kg CO2 e
Scenario 1c: Replacing soya 0.92 −1.04 (−40%) 1.57
Scenario 1d: Replacing rapeseed 0.92 −0.09 (−3%) 2.51
Scenario 2b: Renewable energy 0.92 −0.70 (−27%) 1.91

Figure 2. GHG emissions of Scottish malt whisky production with different end uses of by-products.
Scenarios applying draff only are presented in blue colour and scenarios applying both draff and pot
ale in red colour. Scenario 1a: draff replacing soya bean meal and barley, Scenario 1b: draff replacing
rapeseed meal and barley, Scenario 1c: DDGS replacing soya bean meal and barley, Scenario 1d: DDGS
replacing rapeseed meal and barley, Scenario 2a: draff replacing grid electricity and oil and Scenario
2b: draff + pot ale replacing grid electricity and oil.

The sensitivity analysis shows that the method used for quantifying the GHG emissions associated
with the land use changes has a major effect on the comparison between different uses of the
by-products and on conclusions drawn from this comparison. It can be seen in Table 8 that when
lower LUC emissions are applied for soya, the benefits of by-product feed use in reduction of the
GHG emissions are largely lost and the use of the by-products for heat and electricity generation
becomes the most efficient option. In fact, in the option where zero LUC emissions were assigned to
soya production, the use of DDGS to replace soya became the least efficient way to reduce the GHG
emissions of whisky production, while in the baseline scenario it resulted in the highest reductions.
Including the carbon sequestration (i.e., changes in soil carbon content as a result of the alternative
uses of the by-products) also affected the results. In general, when such changes were accounted for,
the efficiency of energy generation option in reducing the GHG emissions increased. This is because
the net input of C to soil increases when digestate is used as a fertiliser. However, an increase in
soil carbon was also observed when the by-products were used as animal feed. This increase was a
result of the lower digestibility (i.e., higher proportion of non-digestible carbon compounds per unit of

171
Sustainability 2018, 10, 1473

digestible energy) of the by-products and hence higher dry matter excretion when the by-products
were used as feed, compared to the alternative feed ingredients barley and soya/rapeseed.

Table 8. The results of the sensitivity analysis showing the GHG emissions (kg CO2 e per litre of alcohol)
with different assumptions of land use changes (LUC)-related emissions and carbon sequestration.
Scenario 1a: draff is used to replace soya; Scenario 1b: draff is used to replace rapeseed; Scenario 1c:
DDGS is used to replace soya; Scenario 1d: DDGS is used to replace rapeseed meal; Scenario 2a: draff is
used to replace grid electricity and oil; Scenario 2b: draff and pot ale are used to replace grid electricity
and oil.

Scenario 1a Scenario 1b Scenario 1c Scenario 1d Scenario 2a Scenario 2b

Baseline 1.92 2.36 1.57 2.51 2.21 1.91
Alternative LUC emissions
2.21 2.36 2.21 2.51 2.21 1.91
(Williams et al. 2016)
No LUC emissions 2.44 2.36 2.73 2.51 2.21 1.91
Including carbon sequestration 1.88 2.33 1.53 2.50 2.16 1.83

General Discussion
Overall, the results confirm the expectations of the whisky industry that the carbon footprint
of whisky production can be reduced considerably when the by-products are used to generate
heat and electricity and therefore the use of fossil fuels in the distillation process can be reduced.
However, the by-products can also have other, indirect effects outside the distillery system, affecting
greenhouse gas emissions. To understand and quantify such effects, other systems, in addition to
whisky production itself, need to be included in the analysis and this can be done by applying a
systems-based modelling approach.
In general, when the greenhouse gas emissions related to agricultural by-products (or co-products)
are considered using LCA or other environmental assessment methods, the methodological choices
related to allocation of the environmental burdens between those products often become a central
issue of the analysis. Unfortunately, such choices can be very much subjective and they can also
strongly affect the outcomes of the study in question. In studies related to livestock production and
especially animal feeding, the use of various by-products as feed ingredients has often been found
as an environmentally friendly option [3,36]. The reason for this that amongst different potential
approaches to handling the co-products in environmental impact assessment, economic allocation
has been widely used in agricultural LCA studies [38,39,61]. As an outcome of such analyses, smaller
proportions of the environmental impacts are allocated to low value by-products, compared to the
“main” product. In many cases, such an approach is justified and preferred, keeping in mind that the
main product, not the by-products, is actually the driving force of the production.
Despite the general applicability of the economic allocation, alternative allocation methods have
also been suggested for agricultural LCA. The idea behind this is that the ISO [44] standards prefer
the use of a “causal” or “physical” allocation method, in cases where allocation cannot be avoided
altogether for example through system separation. Another reason for avoiding economic allocation is
the potentially varying prices of the co-products, which has sometimes been considered problematic
and causing inconsistencies in LCA studies. However, alternative methods, such as system separation,
or so called “biophysical allocation”, where the aim is to link the inputs to outputs through actual
physical flows or causalities [61–65] are problematic due to the unique nature of agricultural LCA.
The fact is that agricultural products are always an outcome of complicated biological processes
with various interactions. Therefore, attempts to physically separate the processes behind each
co-product are not meaningful as such an approach would necessarily be based on arbitrary, subjective
decisions [66]. In addition to attempts to model the physical flows, other “physical” allocation methods,
used to avoid economic allocation, can be based for example on mass (fresh or dry matter) or protein
or energy content of the products. Again, using such methods in agricultural LCA in a systematic way

172
Sustainability 2018, 10, 1473

can be very difficult, due to potentially varying end uses of the by-products and possible difficulties in
distinguishing between actual products and waste materials, for example, in case of manure [66].
To avoid allocation, in cases where system separation is not possible, the ISO [44] standards
recommend using a system expansion approach. System expansion is also preferred over co-product
allocation in various carbon footprinting guidelines such as PAS 2050 [50]. Over recent years, this
approach has been widely applied for example in LCA studies on livestock production [67,68].
However, as pointed out by Mackenzie et al. [66], the use of this approach cannot be considered as
becoming a general practice in agricultural LCA, for example due to possible difficulties in identifying
the main product and by-products. Another difficulty with this approach is that it could require
large amount of additional data from other sub-processes or systems [66,69,70]. Despite possible
shortcomings, the use this method can be considered to be justified in many cases and especially
when 1) the process in question is clearly targeted to produce one specific main product and 2) the
focus of the analysis is in alternative uses of the emerging by-products, not in the production process
itself. This was the case in this study and in fact, it would be difficult to systematically compare
the very different uses of whisky by-products by applying any other of those alternative methods
mentioned above.
The system expansion (usually as part of so called “consequential LCA” approach [71]) has
been earlier used in other studies evaluating the environmental consequences of alternative uses
of agricultural by-products, including the use of those products in generating renewable energy.
For example, Styles et al. [57] used a consequential approach to quantify the reduction of the GHG
emissions when manure and food waste are used in AD in a dairy farm. Their conclusion was that the
achieved benefits were dependent on how much crops were used as co-digestate in addition to the
manure, as this would determine the need for animal feed imported to the farm, which had its own
effect on the feed-related GHG emissions. In another study, van Zanten et al. [72] applied consequential
LCA to compare uses of two by-products, namely wheat middlings and beet tails. In the case of the
beet tails, the alternative use also in their study was bioenergy generation using AD, as opposed to
using them as cattle feed.
Williams et al. [59] assessed the effects of alternative end uses of turkey litter on the environmental
impacts of turkey meat production. Also in that study, a system expansion approach was used in order
to compare the use of litter either as a biofuel (used for electricity generation in a large-scale power
plant) or directly as a fertiliser through land spreading. Similarly, as in the current study, the availability
of nutrients for crop production, obtained from the litter, was quantified for both scenarios and the
displacement of the synthetic fertilisers (and the grid energy in the case of bioenergy use) was taken
into account when calculating the total emissions related to turkey production. That study also
demonstrated the potentially significant effect of carbon sequestration on the overall GHG emissions
arising from agricultural production.

4. Conclusions
The most notable reductions of greenhouse gas emissions of whisky production were achieved
when the distillery by-products replaced soya meal, the production of which is associated with land
use changes. When using the by-products to replace alternative feed ingredients, there were changes
also in emissions from enteric fermentation, manure management and the end use of manure and
its potential to replace synthetic fertilisers but these had only minor effect on the overall greenhouse
gas emissions, compared to effect achieved by changes in the production of the feed and related LUC
emissions. Different by-products had different environmental effects when used as livestock feed.
Compared to draff, DDGS could reduce more greenhouse gas emissions related to production of the
replaced feed ingredients but on the other hand, it had higher emissions arising from processing,
especially from drying and pelletizing.
The use of by-products as a source of renewable energy, that is, production and combustion of
biogas, reduced the greenhouse gas emissions by replacing grid electricity and fossil fuels used for

173
Sustainability 2018, 10, 1473

heating. Additional benefits were achieved by using the digestate as a fertiliser and thus replacing
the production of synthetic nitrogen fertilisers. Overall, the energy use of by-products could produce
reduction of greenhouse gas emissions with similar magnitude as the use of the by-products as feed.
It should be also noted that in the case of this study, similarly as in earlier studies on
agricultural by-products discussed above, the outcome is largely dependent on methodological choices.
The sensitivity analysis demonstrates that the calculated reductions in the GHG emissions are strongly
affected by the method how the emissions associated with land use changes and land management are
accounted for in the calculations. Currently, there is no generally accepted approach to this process and
this is causing difficulties in comparing the results of agricultural LCAs, especially in cases where the
products are strongly associated with LUC. In assessment of greenhouse gas emissions in agricultural
production, probably the most important single product where direct LUC is involved is soya bean
meal imported from South America. This has been demonstrated for example by Leinonen et al. [51],
who applied LCA modelling to quantify the environmental impacts of UK poultry production systems
with alternative scenarios using different protein crops as a basis of diet formulations for broilers and
laying hens. The general conclusion of their study was that inclusion of alternative protein sources
(e.g., beans or peas) to replace soya bean meal could slightly reduce the Global Warming Potential of
broiler and egg production but also in that study, this observed reduction was highly dependent on
the LUC emission accounting method.
A high sensitivity to the LUC emissions was also found by van Zanten et al. [72]. According to
their findings, higher reductions in GHG emissions could be achieved with the feed use of beet
tails, through displaced emissions related to barley production, when compared to the bioenergy use.
However, this was only the case when indirect LUC emissions were accounted for in barley productions,
which is not a common practice in agricultural LCA studies [73]. If these emissions were excluded,
higher reductions in the emissions could be achieved through the bioenergy option [72]. To avoid these
methodological problems, some attempts have been made to harmonize the LUC accounting methods
in agricultural LCA [73,74]. Despite this, current inconsistencies in the methods will necessarily remain
a challenge in interpretation of the results of studies on environmental sustainability of agricultural
products, especially in the context of livestock systems.
In addition to carbon losses due to land use changes, agricultural systems can also contribute to
carbon sequestration. Although a large proportion of the carbon in the UK soils has been lost during
recent decades, partly as a result of agricultural practices [75,76], this trend can be partially reversed
for example, by the use of organic fertilisers. Although the changes in soil carbon (other than those
related to land use changes) are not usually considered in agricultural LCA, we explored this process
in the sensitive analysis of this study, using a similar approach as Williams et al. [59]. In general,
soil carbon balance is potentially an important component of the overall effect of agricultural and
bioenergy systems on global GHG emissions and therefore should not be ignored in such studies.

Supplementary Materials: The following supplementary materials are available online at http://www.mdpi.
com/2071-1050/10/5/1473/s1, 1. Diagram of the production systems and material flows, 2. Quantifying GHG
emissions from malt whisky production and 3. Outline of the Scottish Agricultural Emission Model (SAEM).
Author Contributions: All authors contributed to the design of the study, analysis of the data and writing the
paper. I.L. led the writing process and data analysis, M.M. led the development of the livestock modelling tool
and J.B. provided unpublished data for the analysis.
Acknowledgments: This research was undertaken within the Scottish Government Rural Affairs and the
Environment Portfolio Strategic Research Programme 2016–2021, WP 1.4 “Integrated and Sustainable Management
of Natural Assets” and 2.4 “Rural Industries.”
Conflicts of Interest: The authors declare no conflict of interest.

174
Sustainability 2018, 10, 1473

References
1. Woyengo, T.A.; Beltranena, E.; Zijlstra, R.T. Nonruminant Nutrition Symposium: Controlling feed cost by
including alternative ingredients into pig diets: A review. J. Anim. Sci. 2014, 92, 1293–1305. [CrossRef]
[PubMed]
2. Zijlstra, R.T.; Beltranena, E. Swine convert co-products from food and biofuel industries into animal protein
for food. Anim. Front. 2013, 3, 48–53. [CrossRef]
3. Mackenzie, S.G.; Leinonen, I.; Ferguson, N.; Kyriazakis, I. Can the environmental impact of pig systems be
reduced by utilising co-products as feed? J. Clean. Prod. 2016, 115, 172–181. [CrossRef]
4. Nonhebel, S. Energy from agricultural residues and consequences for land requirements for food production.
Agric. Syst. 2007, 94, 586–592. [CrossRef]
5. Ajila, C.M.; Brar, S.K.; Verma, M.; Tyagi, R.D.; Godbout, S.; Valéro, J.R. Bio-processing of agro-byproducts to
animal feed. Crit. Rev. Biotechnol. 2012, 32, 382–400. [CrossRef] [PubMed]
6. Dhiman, T.R.; Bingham, H.R.; Radloff, H.D. Production response of lactating cows fed dried versus wet
brewers’ grain in diets with similar dry matter content. J. Dairy Sci. 2003, 86, 2914–2921. [CrossRef]
7. Miyazawa, K.; Sultana, H.; Hirata, T.; Kanda, S.; Itabashi, H. Effect of brewer’s grain on rumen fermentation,
milk production and milk composition in lactating dairy cows. Anim. Sci. J. 2007, 78, 519–526. [CrossRef]
8. Chiou, P.W.S.; Chen, C.R.; Chen, K.J.; Yu, B. Wet brewers’ grains or bean curd pomance as partial replacement
of soybean meal for lactating cows. Anim. Feed Sci. Technol. 1998, 74, 123–134. [CrossRef]
9. Gallo, M.; Sommer, A.; Mlynar, R.; Rajcakova, L. Effect of dietary supplementation with brewery draff on
rumen fermentation and milk production in grazing dairy cows. J. Farm. Anim. Sci. 2001, 34, 107–113.
10. Mussatto, S.I.; Dragone, G.; Roberto, I.C. Brewers’ spent grain: Generation, characteristics and potential
applications. J. Cereal Sci. 2006, 43, 1–14. [CrossRef]
11. Belibasakis, N.G.; Tsirgogianni, D. Effects of wet brewers grains on milk yield, milk composition and blood
components of dairy cows in hot weather. Anim. Feed Sci. Technol. 1996, 57, 175–181. [CrossRef]
12. Sawadogo, L.; Sepehri, H.; Houdebine, L.M. Presence of a factor stimulating prolactin and growth hormone
secretion in brewers’ spent grains. Reprod. Nutr. Dev. 1989, 29, 139–146. [CrossRef] [PubMed]
13. Yaakugh, I.D.I.; Tegbe, T.S.B.; Olorunju, S.A.S.; Aduku, A.O. Replacement value of brewers’ dried grain for
maize on performance of pigs. J. Sci. Food Agric. 1994, 66, 465–471. [CrossRef]
14. Dung, N.N.X.; Manh, L.H.; Udén, P. Tropical fibre sources for pigs—Digestibility, digesta retention and
estimation of fibre digestibility in vitro. Anim. Feed Sci. Technol. 2002, 102, 109–124. [CrossRef]
15. Gutierrez, N.A.; Kil, D.Y.; Liu, Y.; Pettigrew, J.E.; Stein, H.H. Effects of co-products from the corn-ethanol
industry on body composition, retention of protein, lipids and energy and on the net energy of diets fed to
growing or finishing pigs. J. Sci. Food Agric. 2014, 94, 3008–3016. [CrossRef] [PubMed]
16. Stein, H.H.; Shurson, G.C. Board-invited review: The use and application of distillers dried grains with
solubles in swine diets. J. Anim. Sci. 2009, 87, 1292–1303. [CrossRef] [PubMed]
17. Duttlinger, A.J.; Derouchey, J.M.; Tokach, M.D.; Dritz, S.S.; Goodband, R.D.; Nelssen, J.L.; Houser, T.A.;
Sulabo, R.C. Effects of increasing crude glycerol and dried distillers grains with solubles on growth
performance, carcass characteristics and carcass fat quality of finishing pigs. J. Anim. Sci. 2012, 90, 840–852.
[CrossRef] [PubMed]
18. Graham, A.B.; Goodband, R.D.; Tokach, M.D.; Dritz, S.S.; Derouchey, J.M.; Nitikanchana, S.; Updike, J.J. The
effects of low-, medium- and high-oil distillers dried grains with solubles on growth performance, nutrient
digestibility and fat quality in finishing pigs. J. Anim. Sci. 2014, 92, 3610–3623. [CrossRef] [PubMed]
19. Olumu, J.M. Industrial by-products as alternative to maize in ration. Anim. Sci. J. 1988, 15, 61–63.
20. Carias, D.; Millan, N. Brewery waste as a substitute for soy protein in soy-brewer’s yeast mixtures to feed
broiler chickens. Arch. Latinoam. Nutr. 1996, 46, 67–70. [PubMed]
21. Onifade, A.A.; Babatunde, G.M. Comparison of the utilization of palm kernel meal, brewer’s dried grains
and maize offal by broiler chicks. Br. Poult. Sci. 1998, 39, 245–250. [CrossRef] [PubMed]
22. Kratzer, F.H.; Earl, L. The feeding value of the protein of brewers’ dried grains for chicks. Poult. Sci. 1980, 59,
2361–2364. [CrossRef]
23. Swain, B.K.; Naik, P.K.; Chakurkar, E.B.; Singh, N.P. Effect of feeding brewers’ dried grain on the performance
and carcass characteristics of Vanaraja chicks. J. Appl. Anim. Res. 2012, 40, 163–166. [CrossRef]

175
Sustainability 2018, 10, 1473

24. Kaur, V.I.; Saxena, P.K. Incorporation of brewery waste in supplementary feed and its impact on growth in
some carps. Bioresour. Technol. 2004, 91, 101–104. [CrossRef]
25. Muzinic, L.A.; Thompson, K.R.; Morris, A.; Webster, C.D.; Rouse, D.B.; Manomaitis, L. Partial and total
replacement of fish meal with soybean meal and brewers’ grains with yeast in practical diets for Australian
red claw crayfish Cherax quadricarinatus. Aquaculture 2004, 230, 359–376. [CrossRef]
26. Huige, N.J. Brewery by-products and effluents. In Handbook of Brewing; Hardwick, W.A., Ed.; Marcel Dekker:
New York, NY, USA, 1994; pp. 501–550. ISBN 9780585139173.
27. Santos, M.; Jiménez, J.J.; Bartolomé, B.; Gómez-Cordovés, C.; del Nozal, M.J. Variability of brewers’ spent
grain within a brewery. Food Chem. 2003, 80, 17–21. [CrossRef]
28. National Research Council. Nutrient Requirements of Swine, 11th ed.; The National Academies Press:
Washington, DC, USA, 2012; ISBN 978-0-309-22423-9.
29. Ghazalah, A.A.; Abd-Elsamee, M.O.; Moustafa, E.S. Use of distillers dried grains with solubles (DDGS) as
replacement for soybean meal in laying hen diets. Int. J. Poult. Sci. 2011, 10, 505–513. [CrossRef]
30. Hoffman, L.A.; Baker, A. Estimating the Substitution of Distillers’ Grains for Corn and Soybean Meal in
the U.S. Feed Complex. Economic Research Service/USDA. Available online: https://www.ers.usda.gov/
publications/pub-details/?pubid=36472 (accessed on 27 April 2018).
31. Guo, L.B.; Gifford, R.M. Soil carbon stocks and land use change: A meta analysis. Glob. Chang. Biol. 2002, 8,
345–360. [CrossRef]
32. Soya and the Cerrado: Brazil’s Forgotten Jewel. WWF Report UK 2012. Available online: http://assets.wwf.
org.uk/downloads/soya_and_the_cerrado.pdf (accessed on 27 April 2018).
33. Clay, J. World Agriculture and the Environment, 4th ed.; Island Press: Washington, DC, USA, 2003; ISBN
9781559633703.
34. Economic Report on Scottish Agriculture. Available online: http://www.gov.scot/Topics/Statistics/Browse/
Agriculture-Fisheries/PubEconomicReport (accessed on 26 March 2018).
35. Bell, J.; Morgan, C.; Dick, G.; Reid, G. Distillery Feed By-Products Briefing, An AA211 Special Economic
Study for the Scottish Government. 2012. Available online: http://www.sruc.ac.uk/download/downloads/
id/1057/distillery_feed_by-products_briefing (accessed on 26 March 2018).
36. Meul, M.; Ginneberge, C.; Van Middelaar, C.E.; de Boer, I.J.M.; Fremaut, D.; Haesaert, G. Carbon footprint of
five pig diets using three land use change accounting methods. Livest. Sci. 2012, 149, 215–223. [CrossRef]
37. De Vries, M.; de Boer, I.J.M. Comparing environmental impacts for livestock products: A review of life cycle
assessments. Livest. Sci. 2010, 128, 1–11. [CrossRef]
38. Ardente, F.; Cellura, M. Economic allocation in life cycle assessment. J. Ind. Ecol. 2012, 16, 387–398. [CrossRef]
39. Brankatschk, G.; Finkbeiner, M. Application of the Cereal Unit in a new allocation procedure for agricultural
life cycle assessments. J. Clean. Prod. 2014, 73, 72–79. [CrossRef]
40. Scots Whisky Association. Environmental Strategy. Available online: http://www.scotch-whisky.org.uk/
what-we-do/environmental-strategy/ (accessed on 26 March 2018).
41. Risberg, K.; Cederlund, H.; Pell, M.; Arthurson, V.; Schnürer, A. Comparative characterization of digestate
versus pig slurry and cow manure—Chemical composition and effects on soil microbial activity. Waste Manag.
2017, 61, 529–538. [CrossRef] [PubMed]
42. Ohdoi, K.; Miyahara, S.; Iwashita, K.; Umeda, M.; Shimizu, H.; Nakashima, H.; Miyasaka, J. Optimization
of fertiliser application schedule: Utilization of digestate after anaerobic digestion as liquid fertiliser.
IFAC Proc. Vol. 2013, 46, 317–322. [CrossRef]
43. Scottish Tenant Farmers Association News Release, 21st February 2017. Available online:
http://www.tfascotland.org.uk/stfa-urges-government-to-rethink-policy-of-turning-valuable-livestock-
protein-feed-into-renewable-energy/ (accessed on 4 April 2018).
44. BS EN ISO 14044:2006. Environmental Management—Life Cycle Assessment—Requirements and Guidelines.
Available online: https://www.iso.org/standard/38498.html (accessed on 26 March 2018).
45. Eggleston, H.S.; Buendia, L.; Miwa, K.; Ngara, T.; Tanabe, K. (Eds.) 2006 IPCC Guidelines for National
Greenhouse Gas Inventories, Prepared by the National Greenhouse Gas Inventories Programme, Volume 4: Agriculture,
Forestry and Other Land Use; Institute for Global Environmental Strategies (IGES): Hayama, Japan, 2006;
Available online: http://www.ipcc-nggip.iges.or.jp/public/2006gl/index.html (accessed on 26 March 2018).
46. Feedipedia: An On-Line Encyclopedia of Animal Feeds. Available online: https://www.feedipedia.org
(accessed on 26 March 2018).

176
Sustainability 2018, 10, 1473

47. MacLeod, M.; Sykes, A.; Leinonen, I.; Eory, V. Quantifying the Greenhouse Gas Emission Intensity of Scottish
Agricultural Commodities: CXC Project; Technical Report; SRUC: Edinburgh, UK, 2017.
48. Food and Agriculture Organization of the United Nations. Global Livestock Environmental Assessment Model
Version 2.0 Model Description Revision 4, June 2017; Food and Agriculture Organization of the United Nations
(FAO): Rome, Italy, 2017.
49. Global Livestock Environmental Assessment Model (GLEAM). Food and Agriculture Organization of the
United Nations (FAO), Rome. Available online: http://www.fao.org/gleam/en/ (accessed on 26 March 2018).
50. Specification for the Assessment of the Life Cycle Greenhouse Gas Emissions of Goods and Services. PAS
2050:2011. Available online: http://www.bsigroup.com/Standards-and-Publications/How-we-can-help-
you/Professional-Standards-Service/PAS-2050/ (accessed on 26 March 2018).
51. Leinonen, I.; Williams, A.G.; Waller, A.H.; Kyriazakis, I. Comparing the environmental impacts of alternative
protein crops in poultry diets: The consequences of uncertainty. Agric. Syst. 2013, 121, 33–42. [CrossRef]
52. De Vries, J.W.; Vinken, T.M.W.J.; Hamelin, L.; de Boer, I.J.M. Comparing environmental consequences
of anaerobic mono- and co-digestion of pig manure to produce bio-energy—A life cycle perspective.
Bioresour. Technol. 2012, 125, 239–248. [CrossRef] [PubMed]
53. Jenssen, T.K.; Kongshaug, G. Energy Consumption and Greenhouse Gas Emissions in Fertiliser Production;
Proceedings No. 509; The International Fertilizer Society: York, UK, 1998.
54. Greenhouse Gas Reporting—Conversion Factors 2016. Department for Business, Energy & Industrial
Strategy, UK. Available online: https://www.gov.uk/government/publications/greenhouse-gas-reporting-
conversion-factors-2016 (accessed on 26 March 2018).
55. Luna-delRisco, M.; Normak, A.; Orupõld, K. Biochemical methane potential of different organic wastes and
energy crops from Estonia. Agron. Res. 2011, 9, 331–342.
56. Eory, V.; MacLeod, M.; Topp, C.F.E.; Rees, R.M.; Webb, J.; McVittie, A.; Wall, E.; Borthwick, F.; Watson, C.;
Waterhouse, A.; et al. Review and Update the UK Agriculture Marginal Abatement Cost Curve to Assess the
Greenhouse Gas Abatement Potential for the 5th Carbon Budget Period and to 2050; Final Report Submitted for
the Project Contract “Provision of Services to Review and Update the UK Agriculture MACC and to Assess
Abatement Potential for the 5th Carbon Budget Period and to 2050”; Committee on Climate Change: London,
UK, 2015.
57. Styles, D.; Gibbons, J.; Williams, A.P.; Stichnothe, H.; Chadwick, D.R.; Healey, J.R. Cattle feed or bioenergy?
Consequential life cycle assessment of biogas feedstock options on dairy farms. GCB Bioenergy 2015, 7,
1034–1049. [CrossRef]
58. Knowledge Reference for National Forest Assessments—Modeling for Estimation and Monitoring. Food
and Agriculture Organization of the United Nations (FAO), Rome. Available online: http://www.fao.org/
forestry/8758/en/ (accessed on 26 March 2018).
59. Williams, A.G.; Leinonen, I.; Kyriazakis, I. Environmental benefits of using turkey litter as a fuel instead of a
fertiliser. J. Clean. Prod. 2016, 113, 167–175. [CrossRef]
60. Electricity Generation Mix by Quarter and Fuel Source (GB). Office of Gas and Electricity Markets (Ofgem).
Available online: https://www.ofgem.gov.uk/data-portal/electricity-generation-mix-quarter-and-fuel-
source-gb (accessed on 26 March 2018).
61. Van der Werf, H.M.G.; Nguyen, T.T.H. Construction cost of plant compounds provides a physical relationship
for co-product allocation in life cycle assessment. Int. J. Life Cycle Assess. 2015, 20, 777–784. [CrossRef]
62. Eady, S.; Carre, A.; Grant, T. Life cycle assessment modelling of complex agricultural systems with multiple
food and fibre co-products. J. Clean. Prod. 2012, 28, 143–149. [CrossRef]
63. Thoma, G.; Jolliet, O.; Wang, Y. A biophysical approach to allocation of life cycle environmental burdens for
fluid milk supply chain analysis. Int. Dairy J. 2013, 31, S41–S49. [CrossRef]
64. Gac, I.A.; Salou, T.; Espagnol, S.; Ponchant, P.; Dollé, J.-B.; van der Werf, H.M.G. An original way of handling
coproducts with a biophysical approach in LCAs of livestock systems. In Proceedings of the 9th International
Conference on Life Cycle Assessment in the Agri-Food Sector (LCA Food 2014), San Francisco, CA, USA,
8–10 October 2014; Schenck, R., Huizenga, D., Eds.; ACLCA: Vashon, WA, USA, 2014; pp. 443–449.
65. Wiedemann, S.G.; Ledgard, S.F.; Henry, B.K.; Yan, M.-J.; Mao, N.; Russell, S.J. Application of life cycle
assessment to sheep production systems: Investigating co-production of wool and meat using case studies
from major global producers. Int. J. Life Cycle Assess. 2015, 20, 463–476. [CrossRef]

177
Sustainability 2018, 10, 1473

66. Mackenzie, S.G.; Leinonen, I.; Kyriazakis, I. The need for co-product allocation in the Life Cycle Assessment
of agricultural systems—Is “biophysical” allocation progress? Int. J. Life Cycle Assess. 2017, 22, 128–137.
[CrossRef]
67. Cederberg, C.; Stadig, M. System Expansion and Allocation in Life Cycle Assessment of Milk and Beef
Production. Int. J. LCA 2003, 8, 350–356. [CrossRef]
68. Wiedemann, S.; Yan, M. Livestock meat processing: Inventory data and methods for handling co-production
for major livestock species and meat products. In Proceedings of the 9th International Conference on Life
Cycle Assessment in the Agri-Food Sector (LCA Food 2014), San Francisco, CA, USA, 8–10 October 2014;
Schenck, R., Huizenga, D., Eds.; ACLCA: Vashon, WA, USA, 2014; pp. 1512–1520.
69. Parker, G. Measuring the environmental performance of food packaging: Life cycle assessment.
In Environmentally Compatible Food Packaging; Chiellini, E., Ed.; Woodhead Publishing Ltd.: Cambridge, UK,
2008; pp. 211–237, ISBN 9781845691943.
70. Curran, M.A. Nanomaterials life cycle assessment: Framing the opportunities and challenges. In Life Cycle
Analysis of Nanoparticles; Vaseashta, A., Ed.; DEStech Publications Inc.: Lancaster, UK, 2015; pp. 24–55,
ISBN 978-1-60595-023-5.
71. Ekvall, T.; Weidema, B.P. System boundaries and input data in consequential life cycle inventory analysis.
Int. J. LCA 2004, 9, 161–171. [CrossRef]
72. Van Zanten, H.H.E.; Mollenhorst, H.; de Vries, J.W.; van Middelaar, C.E.; van Kernebeek, H.R.J.; de Boer, I.J.M.
Assessing environmental consequences of using co-products in animal feed. Int. J. Life Cycle Assess. 2014, 19,
79–88. [CrossRef]
73. Leinonen, I.; Williams, A.G.; Kyriazakis, I. Evaluating methods to account for the greenhouse gas emissions
from Land Use Changes in agricultural LCA. In Proceedings of the 9th International Conference on Life
Cycle Assessment in the Agri-Food Sector (LCA Food 2014), San Francisco, CA, USA, 8–10 October 2014;
Schenck, R., Huizenga, D., Eds.; ACLCA: Vashon, WA, USA, 2014; pp. 711–717.
74. Williams, A.G.; Dominguez, H.; Leinonen, I. A simple approach to land use change emissions for global crop
commodities reflecting demand. In Proceedings of the 9th International Conference on Life Cycle Assessment
in the Agri-Food Sector (LCA Food 2014), San Francisco, CA, USA, 8–10 October 2014; Schenck, R.,
Huizenga, D., Eds.; ACLCA: Vashon, WA, USA, 2014; pp. 1527–1534.
75. Bellamy, P.H.; Loveland, P.J.; Bradley, R.I.; Lark, R.M.; Kirk, G.J.D. Carbon losses from all soils across England
and Wales 1978–2003. Nature 2005, 437, 245–248. [CrossRef] [PubMed]
76. Smith, P.; Chapman, S.J.; Scott, W.A.; Black, H.I.; Wattenbach, M.; Milne, R.; Campbell, C.D.; Lilly, A.;
Ostle, N.; Levy, P.E.; et al. Climate change cannot be entirely responsible for soil carbon loss observed in
England and Wales, 1978–2003. Glob. Chang. Biol. 2007, 13, 2605–2609. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

178
 sustainability

Article
Influence of Reduced Protein Content in Complete
Diets with a Consistent Arginine–Lysine Ratio on
Performance and Nitrogen Excretion in Broilers
Cristina Ullrich 1 , Marion Langeheine 2 , Ralph Brehm 2 , Venja Taube 3 , Diana Siebert 4 and
Christian Visscher 1, *
1 Institute for Animal Nutrition, University of Veterinary Medicine Hannover, Foundation,
Bischofsholer Damm 15, D-30173 Hanover, Germany; [email protected]
2 Institute for Anatomy, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15,
D-30173 Hanover, Germany; [email protected] (M.L.);
[email protected] (R.B.)
3 BEST 3 Gefluegelernaehrung GmbH, Ringstrasse 16, D-27239 Twistringen, Germany; [email protected]
4 CJ Europe GmbH, Ober der Röth 4, D-65824 Schwalbach, Germany; [email protected]
* Correspondence: [email protected]; Tel.: +49-511-856-7415

Received: 30 September 2018; Accepted: 19 October 2018; Published: 23 October 2018

Abstract: The current discussion concerning resource-efficient broiler production inevitably leads
to diets with lowered crude protein (CP) levels. Therefore, the hypothesis was formed that crude
protein reduction far below the recommended levels can significantly lower the nitrogen (N) content
in litter, if essential amino acids are added and a constant lysine-arginine ratio is guaranteed. In a
five-week feeding trial, 360 ROSS 308 broilers of both sexes were randomly assigned to four feeding
groups with six replicates each with a standard three-phase feeding program (d 1–7, d 8–14, d 15–35).
The control group was offered a complete diet with a common protein content found in practice
(CP-% as fed; starter: 21.5, grower: 20.5, finisher: 20.0; lysine/arginine: 100/115). In the experimental
diets the lysine/arginine ratio was constant, whereas the protein content was lowered in steps of
1.00 percent each with simultaneous supplementation of growth limiting amino acids. Feeding a diet
with a 2.00 percent reduced protein content led to higher body weights after 34 days compared to
the control (2329 g vs. 2192 g). The N content in the total litter decreased significantly with a 2.00
and 3.00 percent reduction in the CP content (51.2 vs. 46.2 or rather 36.2 g/kg dry matter (DM)).
Meticulous balanced protein-reduced diets therefore allow a significant environmental relief.

Keywords: arginine; broiler; crude protein; lysine; nitrogen; resource efficiency

1. Introduction
The impact of livestock production on the environment is significant [1–4]. Due to the
intensification of pig and poultry production, owing to efficiency, environmental problems occurred in
some areas of the world [5,6]. Differences in environmental impact among different production systems
(e.g., pork, chicken and beef) can be explained by the following three factors: feed efficiency, differences
in enteric CH4 emission between monogastric animals and ruminants, and differences in reproduction
rates [1,7]. The production of 1 kg of beef protein also has the highest impact, followed by pork
protein, whereas chicken protein has the lowest impact when only meat production is considered [1,8].
Although feed is the primary input source of nutrients, the amount of nutrients ultimately emitted
into the environment is dependent on the efficiency of nutrient utilization of the animal [2,5].
Low protein diets with the correct amino acid (AA) supplementation promote a reduction in N
excretion and ammonia emission from the litter of broiler chickens [9]. Reduction in dietary crude

Sustainability 2018, 10, 3827; doi:10.3390/su10113827 179 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3827

protein (CP) content resulted in a 10–27% reduction in the total amount of N excreted during a six-week
broiler rearing period [10]. Low CP diets, namely to supply sufficient amounts of essential AA to
meet the requirements only, can in turn help to decrease the amounts of excess dietary non-essential
AA [11]. Although reducing dietary CP reduces N content and, therefore, pollution potential of the
resulting litter, adverse effects can occur in live performance [11]. In some studies, low protein diets
failed to support equal growth performance of that of high protein control diets [9,12–14]. Feeding
broiler chickens diets containing a high proportion of crystalline amino acids with low intact CP can
cause retarded growth when using diets below 19% CP [15]. In a recent study, crystalline amino
acid supplementation based on a similar amino acid profile could reduce N excretion and foot pad
dermatitis without having any negative effects on growth performance by reducing dietary CP levels
from 19% to 17% of free-range yellow broilers [16].
In particular, arginine is important in broiler nutrition because in uricotelic animals exogenous
arginine is needed for the urea cycle [17,18]. The National Research Council (NRC) recommends
an arginine–lysine ratio of 1.14 (lysine content in diet: 1.10% at 90% dry matter (DM)) for broilers
in the first three weeks of fattening and a ratio of 1.10 in the fourth to sixth week (lysine content in
diet: 1.00% at 90% DM [19]). The information in the literature, however, is not without contradiction.
In younger broilers males optimized body weight gain was found for 1.15% dietary arginine (1.21%
lysine; 20.6% CP; [20]). In older birds, the final body weight together with body weight gain and
feed conversion throughout the 42-to-56-d experimental period were optimized at 0.98% arginine
and 0.85% lysine (ratio = 1.15; [21]). In a preliminary study a constant arginine–lysine ratio of 1.15
in protein was found to be the optimum for broiler nutrition under European conditions during the
starter period [22].
Therefore, the objective of the present study was to evaluate the effects of reduced protein content
in complete diets with a consistent arginine–lysine ratio on performance and N excretion in broilers
during a 34-day rearing period.

2. Materials and Methods

Animal experiments were carried out in accordance with German regulations. These animal
experiments require no notification or approval in accordance with the Animal Protection Act (§ 7,
paragraph 2, sentence 3). Interventions before dissection were not carried out. The animals were killed
in accordance with § 4, paragraph 3 of the Animal Protection Act, exclusively to use their organs or
tissues for scientific purposes. The experiments were approved by the Animal Welfare Officer of the
University of Veterinary Medicine Hannover, Germany (reference: TVT-2018-V-102).

2.1. Animals, Housing and Experimental Design

Experiments were performed with a common line of broilers kept for fattening purposes
(as hatched; ROSS 308; BWE-Brüterei Weser-Ems GmbH & Co. KG; Visbek-Rechterfeld, Germany).
In total 360 one-day-old broiler chickens were divided into four different groups depending on the CP
content or rather reduction in CP content (in steps of 1%) in the diet (n = 4: CP-C, CP-1; CP-2; CP-3;
with six replicates each; 15 animals per replicate/subgroup). If an animal died or showed weakness
during the first two weeks of the trial, it was replaced by a broiler from a reserve group. After that
time, no replacement was made.
From day 1 onwards the animals were kept in 24 boxes (1.20 × 0.80 m; AviMax, Big Dutchman
International GmbH, Vechta-Calveslage, Germany). One subgroup of each group was placed in
a block (=4 boxes) in a randomised sequence, with six blocks in the same stable. A vacuum air
ventilation system was installed in the ceiling in two rows above the pens. The boxes were littered with
approximately 1 cm (1 kg per square metre) of wood shavings (GOLDSPAN® , Goldspan GmbH and
Co. KG, Goldenstedt, Germany). By the end of the trial stocking densities had reached a maximum
of 35 kg per square metre. On the left-hand side of each pen, there was a scratching area, and on the
right-hand side there was a feeding area equipped with one hanging-type feeder (Klaus Gritsteinwerk

180
Sustainability 2018, 10, 3827

GmbH & Co. KG, Bünde, Germany). Drinking lines with nipple drinkers (two nipples per box)
for broilers (Big Dutchman International GmbH, Vechta, Germany) were used. The environmental
temperature was gradually reduced from about 33 ◦ C for the one-day-old birds to about 20 ◦ C by
day 34. Lights were continuously on at days one, two, and three, and the photoperiod from day four
onwards amounted to 16 h of light and 8 h of darkness with dimmed night lighting.

2.2. Diets and Feeding Concept

All birds were fed ad libitum with specifically prepared pelleted diets. For the trial, 12 different
diets (four different starter diets, four grower diets, and four finisher diets) were produced at the
Institute for Animal Nutrition, University of Veterinary Medicine Hannover, Foundation, Hannover,
Germany. One component (80% of diet; Best 3 Geflügelernährung GmbH, Twistringen, Germany)
of each of the 12 diets was the same supplementary feed with vitamins, minerals and coccidiostats
(narasin/nicarbacin). This maximized the comparability of the final diets with each other.
The remaining 20% of the specific compound feedingstuffs consisted of corn, soybean meal,
amino acids and some minerals (limestone, monocalciumphosphate, salt, sodium bicarbonate) to make
up the 12 different experimental diets (Table 1).

Table 1. Ingredient composition of the diets during the whole experimental period. CP: crude protein.

Starter Grower Finisher

Parameter [%]
CP-C CP-1 CP-2 CP-3 CP-C CP-1 CP-2 CP-3 CP-C CP-1 CP-2 CP-3
Supplementary Feedingstuff * 80.0 80.0 80.0 80.0 80.0 80.0 80.0 80.0 80.0 80.0 80.0 80.0
Corn 0.30 4.51 8.83 13.6 4.31 9.44 13.1 9.95 7.15 10.8 15.3 7.77
Soybean meal 14.8 10.8 6.83 2.40 10.8 6.00 2.40 0.00 8.50 5.25 1.00 0.00
Plant oil 3.40 2.68 1.85 1.00 4.15 3.30 2.60 4.35 4.10 3.30 2.50 5.60
Limestone 0.75 0.74 0.73 0.72 0.30 0.29 0.30 0.28 0.05 0.04 0.02 0.00
Mono-Ca-phosphate 0.50 0.57 0.63 0.70 0.25 0.33 0.39 0.52 0.00 0.06 0.13 0.26
Salt 0.12 0.08 0.04 0.00 0.10 0.05 0.02 0.00 0.07 0.04 0.00 0.00
Sodium Bicarbonate 0.00 0.00 0.05 0.00 0.00 0.06 0.11 0.14 0.00 0.05 0.09 0.10
Arginine 0.00 0.12 0.23 0.36 0.00 0.14 0.25 0.35 0.00 0.10 0.22 0.29
Isoleucine 0.00 0.07 0.14 0.21 0.00 0.08 0.15 0.21 0.00 0.06 0.13 0.17
L-Lysine-HCl 0.04 0.17 0.30 0.44 0.04 0.20 0.32 0.42 0.04 0.15 0.29 0.35
L-Methionine 0.03 0.05 0.06 0.08 0.00 0.02 0.04 0.06 0.00 0.01 0.03 0.05
Threonine 0.07 0.13 0.19 0.26 0.05 0.01 0.18 0.24 0.08 0.13 0.19 0.24
Valine 0.00 0.07 0.13 0.20 0.00 0.08 0.14 0.20 0.00 0.05 0.12 0.17
Caolin 0.00 0.00 0.00 0.00 0.00 0.00 0.00 3.32 0.00 0.00 0.00 5.00
* Containing 51.4% wheat, 24.1% soybean meal, 15.0% corn, 5.08% plant oil, 1.30% limestone, 0.94%
mono-Ca-phosphate, 0.70% formic acid, 0.40% Alimet, 0.25% enzyme mixture (phytase, xylanase), 0.25% premix,
0.22% sodium bicarbonate, 0.22% salt, 0.10% lysine, 0.06% betaine (33%); feed additives per kg: 12,500 IU vitamin
A, 6250 IU vitamin D3, 43 mg Vitamin E, 18.7 mg Cu, 25 mg Fe, 87.5 mg Mn, 62.5 mg Zn, 2.5 mg I, 0.37 mg Se,
acetic acid, formic acid, 625 FTU 6-phytase, 3000 U Endo 1,4-ß-xylanase, 62.5 mg narasin, 62.5 mg nicarbacin.

One group received a standard control diet (starter: d 1–7, grower: d 8–14; finisher: d 15–35),
the other groups, specially prepared experimental diets. The control diet was a complete feedingstuff
with a common protein content (as fed; starter: 21.5% CP; grower: 20.5% CP; finisher: 20.0%
CP; each designed for an arginine–lysine ratio of 115:100; Table 2). In the experimental diets,
the arginine–lysine ratio was constant; the protein was lower in steps of 1.00 per cent. The levels of
essential amino acids were held at the same level due to the supplementation of single amino acids.
To ensure the optimum composition and to verify the ratio between the components, these 12 different
diets (in total: four starters, growers and finishers each) were analyzed (Table 2).

181
Sustainability 2018, 10, 3827

Table 2. Concentrations of ingredients and energy content after chemical analysis in the starter,
grower and finisher diets.

Starter Grower Finisher

Item [g/kg; 88% DM]
CP-C CP-1 CP-2 CP-3 CP-C CP-1 CP-2 CP-3 CP-C CP-1 CP-2 CP-3
Crude ash 58.7 56.4 54.4 51.9 50.5 48.6 47.6 73.8 45.4 46.5 43.3 84.4
Crude fat (EE) 78.8 75.3 68.7 64.4 89.8 83.3 79.3 93.7 93.3 83.5 76.4 103
Crude fibre 20.5 19.6 18.5 16.2 19.2 19.1 18.2 18.4 20.7 20.7 19.3 18.2
Crude protein 222 215 202 192 205 194 186 177 199 192 181 170
Nitrogen free extract 1 500 514 536 556 516 535 549 517 522 537 560 504
Starch 335 356 382 410 355 384 406 380 376 385 412 371
Sugar 52.5 51.9 47.2 43.3 48.7 44.6 41.1 37.4 49.1 44.4 39.8 35.8
Calcium 9.67 9.72 9.69 9.67 8.02 7.62 7.59 7.60 6.03 6.04 6.04 6.07
Phosphorus 7.43 6.59 7.25 7.47 6.34 6.42 5.99 6.13 5.77 5.45 5.24 5.31
Potassium 9.85 8.91 8.12 7.29 8.87 7.92 7.22 7.61 8.41 7.73 7.44 8.37
Arginine 14.8 14.8 14.3 14.8 13.5 13.6 14.1 13.6 13.7 13.1 12.8 12.6
Cysteine 2.23 2.28 2.03 2.02 2.24 2.23 2.05 1.84 2.02 2.30 1.97 1.66
Histidine 5.87 5.53 4.76 4.72 5.28 4.98 4.68 4.28 5.22 5.00 4.33 4.04
Isoleucine 9.62 9.42 8.99 9.38 9.24 8.72 9.04 8.73 7.96 8.55 8.18 8.11
Leucine 16.9 16.1 14.6 14.0 16.3 14.7 14.4 12.7 15.5 15.0 13.3 12.5
Lysine 12.8 12.9 12.4 12.6 12.0 11.7 12.3 11.7 11.7 11.4 11.3 10.8
Methionine 5.18 5.73 5.43 5.59 5.04 5.45 5.01 5.00 5.18 5.10 4.70 5.16
Phenylalanine 10.8 10.2 9.04 8.74 10.4 9.30 8.99 7.96 10.1 9.41 8.24 7.66
Threonine 8.30 8.64 8.14 8.64 7.77 6.73 8.18 7.56 7.86 8.11 7.82 7.36
Valine 10.3 10.5 9.86 10.3 9.83 9.47 10.1 9.69 9.30 9.33 9.07 8.85
Metabolizable energy AMEN 2
12.4 12.5 12.5 12.6 12.8 12.9 12.9 12.8 13.2 12.8 12.8 12.8
[MJ/kg DM]
1Nitrogen-free extract = DM − (crude ash + crude fat + crude fibre + crude protein); 2 AMEN = nitrogen-corrected
apparent metabolizable energy; AMEN (per kg) = 0.1551 × % CP + 0.3431 × % ether extracts (EE) + 0.1669 ×
% starch + 0.1301 × % sugar (as sucrose).

2.3. Measurements

2.3.1. Technical Performance

The individual body weight (BW) was measured weekly on the same day. One exception was
the last week, in which the interval had to be shortened by one day for technical reasons (six days).
Feed intakes (FI) as well as losses were determined at subgroup level. The feed conversion ratio (FCR)
was estimated from feed consumed and body weight growth throughout the experimental period at
box level.

2.3.2. Excreta and Litter Sampling

Excreta samples were obtained by means of a rubber mat placed on top of the litter for one hour
in each box once a week. Excreta samples were collected without wood shavings contaminating the
samples. Litter samples for measuring the DM content were collected weekly from three defined
locations along a diagonal line through the box (at both ends and a central one). At each area, over the
whole bedding height a sample was punched out from the full depth of the litter using a cup with
a 5 cm diameter. At the end of the experiment, the entire litter material was removed, weighed
and homogenised with a rotating machine. An aliquot was taken from this material and used for
further analyses.

2.3.3. Foot Pad Dermatitis Scoring Criteria

Foot pads were examined weekly, starting at the end of week one. Dirty feet were carefully
washed with a wet cloth to remove slightly adhering litter and excreta. Only the dried central plantar
of foot pads were scored. The foot pads of the animals were scored with a scoring system from
0–7 designed by Mayne, et al. [23]: score 0 represents healthy skin with no swelling or redness, whereas
score 7 stands for a foot pad more than 50% necrotic (Figure 1). Other measures concerning behaviour,
use of space, use of the sandbox, and other welfare indicators might have been very useful, but were
not part of the study. They should be considered in further studies.

182
Sustainability 2018, 10, 3827

Figure 1. Foot pad lesions with different scores. (a) Score 0: no alterations detected; and (b) Score
7: more than half of the foot pad covered with necrotic cells (photo: ©University of Veterinary
Medicine, Hannover).

2.3.4. Dissection
After 35 days, 120 animals (n = 30 per group) were dissected. A percussive blow to the head was
used as anaesthesia or rather the stunning method in accordance with Annex I of Council Regulation
(EC) No. 1099/2009, Chapter I, Methods, Table 1—Mechanical methods, No. 6. After bleeding the
animals, the body cavity was opened, the sternum lifted up and samples of the ileum were taken for
histological investigations. All remaining birds were sold.

2.3.5. Histological Investigations

For histological investigations, an approximately 1 cm long piece was removed from the ileum
(in the middle between the diverticulum and cranial part of the caecum) and fixed in 4% formaldehyde
for 48 h. After fixation, tissue samples were embedded in paraffin using standard techniques [24].
For histological evaluation, 4 μm sections of all samples were stained with haematoxylin and eosin
(HE) using established protocols [24]. The villus height was measured from the tip of the villi to the
villus crypt junction; villus width was measured at the base of the villus above the villus crypt junction
using a Zeiss axioscope (Carl Zeiss Jena GmbH, Jena, Germany).

2.3.6. Analysis of Feed, Excreta, and Litter Samples

The official methods of the VDLUFA were the basis of the standard procedures being used to
analyze all diets [25]. Determining the dry matter content and the crude ash content works through
action of heat; drying the samples to the weight constancy at 103 ◦ C delivers the results for the DM
content. Through combustion of the sample at 600 ◦ C in a muffle furnace the crude ash content
was analyzed. The total N content was determined by the DUMAS combustion method (Vario Max,
Elementar, Hanau, Germany). The crude fat content was determined by standard protocol (soxhlet
apparatus). Crude fiber was analyzed after washing in dilute acids and alkalis. Starch determination
was carried out polarimetrically (Polatronic E, Schmidt und Haensch GmbH & Co., Berlin, Germany).
The Luff-Schoorl method was used to determine the sugar content. Minerals were analyzed by
atomic absorption spectrometry (Unicam Solaar 116, Thermo, Dreieich, Germany). Amino acids were
determined by ion-exchange chromatography (AA analyzer LC 3000, Biotronic, Maintal, Germany).

2.3.7. Estimations of Efficiencies of Nitrogen or Rather Protein Utilisation

The single box was the observation unit for assessing nutrient efficiency between groups. The basis
for the considerations was the total FI in the box, the increase in body weight (final body weight minus

183
Sustainability 2018, 10, 3827

weight at hatch; including the increase in deceased animals), and the amount of final litter material
in the box. The N content in the different diets and in the litter were analyzed by standard methods
described above (2.2.6). To calculate the N content in the fresh whole body of birds (including feathers),
crude protein contents from various publications were used as a basis [12,26–28]. From the means
(in g N/100 g fresh total body: 3.312 [27], 3.016 [26], 2.754 [28], 2.598 [12]) a factor was derived
(2.920) and used as the basis for calculating parameters in accordance with Aletor, Hamid, Niess and
Pfeffer [26], modified.

N-retention efficiency (%) = g N retained/g N consumed × 100

N-efficiency rate = g weight gain/g N consumed

N excretion (apparent) = g N consumed − g N retained

2.4. Statistical Analysis

Data analyses were performed using the SAS statistical software package version 7.1 (SAS Inst.,
Cary, NC, USA). Mean values, as well as the standard deviation of the mean (standard deviation (SD)),
were calculated for all parameters. The mean footpad dermatitis (FPD) scores were evaluated by using
the mean of both feet. For the values of body weight (BW), the foot pad dermatitis scores and the
results of the histopathological investigations as well as the individuum were the basis of observation.
All other parameters were analyzed at box-level. The group comparisons were performed by one-way
analysis of variance (ANOVA) for independent samples. In general, the Ryan–Einot–Gabriel–Welsch
multiple-range test (REGWQ) was used for multiple pairwise means comparisons between the four
groups. All statements of statistical significance were based on p < 0.05.

3. Results
The experiments ran without complications. From the start of week 3, six out of 360 animals died
(CP-C: 2; CP-1: 1; CP-2: 1; CP-3:2). There was no antibiotic treatment during the trial.

3.1. Technical Performance

Results relating to growth performance of broilers are shown in Table 3. At day 1, the average
weight per chicken was 43.0 g. In broilers, after 34 days of fattening, BW exceeded the performance
goals of the breeding company [29]. At the end of the first and the second week of fattening the BW
already showed significant differences between groups, being lowest in group CP-3 (Table 3). In weeks
three, four, and five, birds in group CP-2 were significantly heavier than in groups CP-C and CP-3.

Table 3. Average body weight and feed conversion ratio (FCR) during the trial (mean ± standard
deviation (SD)).

Item Group Week 1 Week 2 Week 3 Week 4 Week 5 *

CP-C 216 A ± 19.8 535 A ± 58.1 989 B,C ± 116 1589 B,C ± 189 2192 B,C ± 258
Body weight CP-1 218 A ± 16.5 541 A ± 51.7 1004 A,B ± 116 1632 A,B ± 199 2244 A,B ± 275
[in g; end of week] CP-2 217 A ± 15.6 552 A ± 47.1 1034 A ± 106 1678 A ± 182 2329 A ± 266
CP-3 206 B ± 20.1 517 B ± 45.6 956 C ± 99.8 1548 C ± 175 2131 C ± 244
CP-C 0.987 ± 0.073 1.169 ± 0.023 1.363 ± 0.043 1.488 ± 0.039 1.848 ± 0.066
CP-1 0.952 ± 0.034 1.185 ± 0.025 1.342 ± 0.026 1.474 ± 0.026 1.817 ± 0.020
FCR [Ø in week]
CP-2 0.996 ± 0.044 1.165 ± 0.009 1.334 ± 0.047 1.494 ± 0.032 1.776 ± 0.050
CP-3 1.025 ± 0.070 1.199 ± 0.042 1.389 ± 0.047 1.518 ± 0.026 1.827 ± 0.104
A,B,C averages differ significantly within a column (p < 0.05); * only six days—measurement end of day 34.

No differences were observed concerning the feed conversion rate (FCR) in broilers depending
on the dietary feeding concept. The FCR showed numerically lowest values for group CP-2 during
the entire period (CP-C: 1.474 ± 0.036; CP-1: 1.457 ± 0.010; CP-2: 1.454 ± 0.017; CP-3: 1.489 ± 0.016,
respectively).

184
Sustainability 2018, 10, 3827

3.2. Excreta and Litter Quality

There were no differences in DM content of excreta between groups CP-C, CP-1 and CP-2 (Table 4).
Excreta of group CP-3 were the driest from week two onwards. The control group had the wettest
litter in the fourth week of fattening. At the end of the experiment, groups CP-C, CP-1 and CP-2 were
not significantly different concerning DM content in litter. The group CP-3 had the driest litter at week
five. The litter material was finally removed from the boxes. The dry matter content was significantly
higher in material from group CP-3 than in the other groups (in g DM/kg; CP-C: 584 B ± 31.3; CP-1:
602 B ± 39.7; CP-2: 603 B ± 44.4; CP-3: 698 A ± 30.7, respectively).

Table 4. Dry matter content of excreta and litter material during the five-week trial period (mean ± SD).

Item Group Week 1 Week 2 Week 3 Week 4 Week 5 *

CP-C 188 B ± 8.34 200 B ± 10.8 189 B ± 7.92 188 B ± 9,31 184 B ± 9.46
Dry matter (DM)
CP-1 193 A,B ± 9.27 208 B ± 9.27 188 B ± 6.62 186 B ± 11.9 184 B ± 8.18
excreta †
[in g/kg; end of week] CP-2 199 A,B ± 14.8 207 B ± 12.1 192 B ± 16.9 184 B ± 14.2 181 B ± 8.01
CP-3 206 A ± 9.47 228 A ± 7.25 228 A ± 20.2 232 A ± 2.76 219 A ± 9.77
CP-C 815 ± 36.2 816 B ± 23.9 712 A,B ± 53.8 588 B ± 54.3 609 B ± 69.8
Dry matter litter ‡ CP-1 829 ± 29.3 837 A,B ± 24.6 698 B ± 42.2 596 A,B ± 67.6 610 B ± 31.3
[in g/kg; end of week] CP-2 817 ± 31.5 831 A,B ± 43.9 718 A,B ± 58.0 617 A,B ± 58.0 584 B ± 61.6
CP-3 830 ± 30.7 856 A ± 24.3 763 A ± 49.7 667 A ± 66.7 709 A ± 45.1
A,B averages differ significantly within a column (p < 0.05); * only six days—measurement end of day 34;
† REGWQ-test; ‡ LSD-test.

Analyzing the N content in the excreta showed that diets with lower CP content led to significantly
lower N values in the excreta (Table 5). In comparison to the control, in week 5 the N content was
reduced by 36.6%. Also, the mean N content in the total litter was significantly lower in group CP-3
(36.2 ± 1.64 g/kg DM) than in all other groups. Additionally, group CP-2 (46.2 ± 1.30 g/kg DM)
showed significantly lower concentrations of N in the total litter compared to the material from the
groups CP-1 (49.7 ± 1.57 g/kg DM) and CP-C (51.2 ± 2.22 g/kg DM).

Table 5. Nitrogen content in excreta during the five-week trial period (mean ± SD).

Item Group Week 1 Week 2 Week 3 Week 4 Week 5

CP-C 44.7 A ± 2.16 43.5 A ± 1.45 44.8 A ± 1.28 46.3 A ± 1.43 50.0 A ± 3.13
Nitrogen content CP-1 43.4 A,B ± 2.05 38.7 B ± 0.71 42.1 B ± 1.79 45.0 A ± 1.59 47.9 A ± 3.02
[in g/kg DM; end of week] CP-2 40.4 A,B ± 2.12 36.4 C ± 2.01 36.4 C ± 2.56 41.2 B ± 1.94 42.4 B ± 2.64
CP-3 35.4 C ± 3.03 29.1 D ± 0.86 28.4 D ± 1.29 29.7 C ± 1.63 31.7 C ± 1.99
A,B,C averages differ significantly within a column (p < 0.05).

The level of FI and the protein content in the feed determined the average total N intake per
box. The birds in group CP-2 showed the significantly highest FI compared to groups CP-1 and CP-3
(per animal; CP-C: 3169 B g, CP-1: 3210 A,B g; CP-2: 3323 A g; CP-3 3107 C g, respectively). Total N
uptake was significantly higher in the control group than in CP-2 and CP-3 (Table 6). The total amount
of N in the litter material harvested at the end of the experiment was gradually reduced analogous to
the protein reduction in the feed. The group CP-2 showed the highest absolute weight gain per box
and accordingly the highest absolute N retention per box compared to the other groups.

Table 6. Estimations of nitrogen balance over the entire trial period (mean ± SD).

N-Intake From N-Amount in Weight Gain Δ N-Retained

Group
Feed [g/box] Final Litter [g/box] Final-Start [g/box] [g/box]
CP-C 1517 A ± 52.5 581 A ± 39.6 32,033 B,C ± 781 938 B ± 22.8
CP-1 1484 A,B ± 52.9 522 B ± 28.2 32,923 A,B ± 1147 938 B ± 22.9
CP-2 1451 B ± 35.8 477 C ± 25.3 34,190 A ± 987 1001 A ± 28.8
CP-3 1278 C ± 30.8 416 D ± 20.0 31,220 C ± 803 914 B ± 23.5
A,B,C,D averages differ significantly within a column (p < 0.05).

185
Sustainability 2018, 10, 3827

The N retention efficiency in the groups CP-C and CP-1 was significantly worse than in the groups
CP-2 and CP-3 (Table 7). Compared to the control, the efficiency could be improved step by step by 1.4,
7.1 and 9.6 percentage points from CP-1 to CP-3, respectively.

Table 7. Estimations of efficiencies of nitrogen utilization (mean ± SD).

N-Retention N-Efficiency N-Excretion (Apparent) ‡ N-Excretion (Apparent) ‡

Group
Efficiency * [%] Ratio † [g/g] [g/box] [g/animal]
CP-C 61.9 C ± 1.46 21.1 D ± 0.50 579 A ± 39.8 38.6 A ± 2.66
CP-1 63.3 C ± 2.76 22.2 C ± 0.17 546 A ± 56.7 36.4 A ± 3.78
CP-2 69.0 B ± 0.81 23.6 B ± 0.28 450 B ± 15.2 30.0 B ± 1.01
CP-3 71.5 A ± 0.70 24.4 A ± 0.24 364 C ± 12.6 24.2 C ± 0.84
A,B,C,D
averages differ significantly within a column (p < 0.05). * Nitrogen retention efficiency (%) = (g N retained/g
N consumed) × 100; † Nitrogen efficiency rate = g weight gain/g N consumed; ‡ Nitrogen excretion (apparent) = g
N consumed − g N retained.

3.3. Footpad Dermatitis

In this trial there were no clinical issues concerning foot pad health. The foot pad health was very
good overall (Table 8). A comparison between groups showed significant differences at the end of the
third week. In group CP-2, the scores were significantly higher.

Table 8. Foot pad (FPD) scores in broilers during the five-week trial period (mean ± SD).

Item Group Week 1 Week 2 Week 3 Week 4 Week 5

CP-C 0.04 ± 0.13 0.46 ± 0.38 0.94 B ± 0.20 0.97 ± 0.15 0.68 ± 0.39
FPD Scores CP-1 0.03 ± 0.12 0.43 ± 0.37 1.02 A,B ± 0.23 0.97 ± 0.12 0.61 ± 0.41
[averages of both feet; end of week] CP-2 0.05 ± 0.17 0.38 ± 0.37 1.04 A ± 0.23 0.97 ± 0.12 0.63 ± 0.40
CP-3 0.03 ± 0.12 0.45 ± 0.38 0.99 A,B ± 0.28 1.01 ± 0.12 0.74 ± 0.41
A,B averages differ significantly within a column (p < 0.05).

3.4. Histological Investigations

There were no differences in the results of the histological examinations (Table 9).

Table 9. Average villus height * and villus width in the ileum of broilers (mean ± SD).

Item Group Dissection

CP-C 454 ± 68.3
CP-1 448 ± 58.1
Villus height * [in μm]
CP-2 455 ± 50.4
CP-3 446 ± 75.9
CP-C 139 ± 23.0
CP-1 142 ± 18.1
Villus width † [in μm]
CP-2 140 ± 26.9
CP-3 140 ± 25.8
* Villus height was measured from the tip of the villi to the villus crypt junction; † villus width was measured at the
base of the villus above the villus crypt junction.

The intestinal wall of the ileum showed no alterations (Figure 2).

186
Sustainability 2018, 10, 3827

Figure 2. HE staining from ileal intestinal wall of broiler chickens with CP-1 diet. Scale bars = 500 μm.

4. Discussion
The investigations were conducted without incidents. Animal losses were very low (1.66%
mortality) from day 14 onwards. Performance parameters were above performance goals of the
breeding company [29]. With a final average body weight between 2131 g (CP-3) and 2329 g (CP-2),
the body weight development excelled the guidelines of the breeding organization (2050 g). Thus,
the performance was higher in each group (CP-C: +6.93%; CP-1: +9.46%; CP-2: +13.6%; CP-3: +3.95%,
respectively). Moreover, the feed utilization per kg body weight gain was lower in all groups compared
to the performance goals (cumulative feed expenditure in accordance with Aviagen [29]: 1528;
reduction: CP-C: −3.53%; CP-1: −4.65%; CP-2: −4.84%; CP-3: −2.55%, respectively). Moran et al. [11]
observed in early studies on CP reduction (downwards to 17.8%; weeks 4–6) an increase in feed to gain
ratio from 1.72 to 1.76. However, the rations were balanced only with L-lysine HCl, DL-methionine,
and L-threonine. The arginine–lysine ratio was therefore not optimal, this being 1.04 in the first three
weeks (20.8% CP) and 0.99 in weeks 4–6 (17.8% CP). In a frequently cited study by Bregendahl et al. [12],
the performance deteriorated when reducing the protein content to a level comparable to ours in
the present study. In the study mentioned above [12], at protein levels of 185–186.5 g CP per kg
diet and supplementation of identical amino acids used in our study, complemented by glutamine,
the performance was lower compared to the control (23% CP). Nonetheless, the two investigations
differ in terms of the absolute levels of supplemented amino acids. Especially methionine seemed
to be much higher in the study of Bregendahl et al. [12]. Namroud et al. [15] were able to show a
comparable body weight in broilers using crystalline amino acids in protein reduced diets (reduction of
23% to 19% CP at day 28). A further reduction to 17% CP led to a significant decrease in the final body
weight at day 28 by 17.5%. In comparison to Namroud et al. [15], no comparable effect occurred in
the present study, although reduction in CP content was nearly the same (a decrease to 17.7% percent
by day 14 or to 17% thereafter). The greatest difference between Namroud et al. [15] and the present
trial can be seen in the methionine content (approx. 1 g higher for Namroud et al. [15]), and leucine
(up to 5 g surplus in the study of Namroud et al. [15]). In studies with free-range chickens, however,
observations were in line with the present study [16]. The performance was comparable when reducing

187
Sustainability 2018, 10, 3827

from 19% to 17% CP and balancing essential amino acid content. From these observations, it can be
concluded that with increasing crude protein reduction, the targeted application of certain amino
acids must be given more emphasis if performance is to be maintained. Feed costs represent about
70% of the cost of poultry production [30]. Therefore, this makes a bird’s ability to use feed efficiently
very important [30]. Precisely following the nutritional requirements of poultry is the guarantor for
optimum feed efficiency [30]. Therefore, studies like this can help to maintain profitability while at the
same time taking into account other aspects of sustainability like ecological dimensions of production.
In the present investigations, the N content in the excreta could be lowered significantly using CP
reduced diets. The N content in the excreta was reduced by up to 36.6% at a comparable performance
by reducing the protein content from 20% to 17% (reduction in N content in excreta compared to
CP-C in week 5: CP-1: −4.20%; CP-2: −15.2%; CP-3: −36.6%, respectively). The ratios were also
reflected in the content of the entire litter material. The protein reduction of up to 3% starting from
a diet with moderate protein content in the present study resulted in a reduction in the N content
in the total litter material of up to 37.3% (N reduction in litter compared to CP-C: CP-1: −5.70%;
CP-2: −22.3%; CP-3: −37.3%, respectively). The N efficiency could be further increased by almost 10
percentage points (CP-C: 61.9%; CP-3: 71.5%, respectively) due to the feeding concept, in spite of an
already high efficiency. The present investigations are in line with the results of Ospina-Rojas et al. [9].
This research group was able to reduce the N content in the litter from 47.2 g N/kg DM to 31.9 g N/kg
DM (−32.4%) by reducing the protein content in the diet from 19% to 16% by supplementing valine,
isoleucine, arginine and glycine achieving a constant performance. When supplementation of valine,
isoleucine and glycine or valine, isoleucine and arginine or of all four aforementioned amino acids
was not made, a significant performance depression occurred [9]. Blair et al. [10] were able to achieve
a reduction in the N content in the excreta from 52.5 g/kg DM to 47.2 g/kg DM without affecting
the performance by reducing the protein contents from 21% to 18% in weeks 3 to 6 while balancing
essential amino acids. The N retention could be increased from 47% to 51%. In the same study, the N
retention could be increased from 61% to 63% under conditions of a total of 6 weeks’ adjustment in
the protein content. Namroud et al. [15] were able to reduce the N content in excreta from 50.3 g/kg
DM to 36.3 g/kg DM (−27.8%) by achieving a constant amino acid content in the diet, reducing the
crude protein content from 23% to 17%. Shao et al. [16] were able to reduce the N content in the
excreta from 65.2 g/kg DM to 47.3 g/kg DM (−27.4%) in free-range chickens by reducing the protein
content from 19% to 17%. In the present investigations, the reduction in the N content in excreta or
litter material was higher in its peak than in the aforementioned publications. Overall, the protein
reduction was accompanied to a certain extent by an increased performance (CP-2), which was also
reflected in the high absolute N efficiency. The current global production of ammonia, CH4 , and N2 O
by the poultry industry is significant [30]. Improvements in feed conversion ratio have a favorable
effect on environmental emissions and decrease the environmental impact of poultry production [30].
Therefore, the present investigations thus show that the environment can be relieved to the maximum
by continuously optimizing the rations.
In this study, no clinical problems concerning the foot pad health of the broilers could be
determined, independent of CP level in the diets. After 34 days of fattening, nearly 100% of the
broilers had an FPD score ≤1, despite the high stocking density of about 35 kg/m2 . Only one animal
in group CP-C and three animals in group CP-3 had a score of 2 in one foot. Therefore, the results of
this study show neither negative nor positive effects of using the different dietary concepts.
The results of the histological examination were used to check whether the reduction in the protein
content also had an influence on intestinal histology. The results of the study gave no indication of this.
With maximum protein reduction (CP-3), we used a diet containing kaolin at the beginning
of the third fattening week effectuating a dilution of the ration. Due to the kaolin the effect of
differences in diet composition between the feeding phases and between the groups in one feeding
phase (80% supplement concept) was minimized. However, it cannot be ruled out that this ingredient
might have influenced the FI. The results of the investigations suggest that further analyses would

188
Sustainability 2018, 10, 3827

be useful. In these investigations the use of kaolin should be avoided on the one hand. Furthermore,
it should be examined to what extent very expensive amino acids such as isoleucine etc. have to
be completely balanced in the rations. If reductions are possible, this would allow the already
economical concept to be continuing optimized and at the same time the environmental burden could
be further reduced.

5. Conclusions
The potential environmental impact is an important evaluation factor for the sustainability of
animal production. Meticulous balanced protein-reduced diets allow a significant reduction in the
use of nutrients, especially in high N containing components. Under these conditions, the adjustment
of the amino acid content becomes more and more important if the performance is at least kept
constant. As the degree of crude protein reduction increases, N excretion falls disproportionately.
This nutritional intervention enables significant improvements in terms of the environmental impact
of animal production.

Author Contributions: Conceptualization, C.V., V.T. and D.S.; Methodology, C.V., M.L. and R.B.; Validation, C.V.,
C.U., M.L. and R.B.; Formal Analysis, C.U. and C.V.; Investigation, C.U., M.L. and C.V.; Resources, C.V., V.T. and
R.B.; Data Curation, C.U. and C.V.; Writing—Original Draft Preparation, C.U. and C.V.; Writing—Review &
Editing, C.U., M.L., R.B., V.T., D.S. and C.V.; Visualization, C.U., C.V., M.L. and R.B.; Supervision, C.V. and R.B.;
Project Administration, C.V. and R.B.; Funding Acquisition, C.V.
Funding: The study was financially supported by CJ Europe GmbH, Schwalbach, Germany. The role of the
funding body was merely financial. The CJ Europe GmbH did not have any role in collecting, interpreting,
analyzing or writing up the data. This publication was also supported by the Deutsche Forschungsgemeinschaft
and University of Veterinary Medicine Hannover, Foundation, Germany within the funding program Open
Access Publishing.
Acknowledgments: We would like to thank Frances Sherwood-Brock for proof-reading the manuscript to ensure
correct English.
Conflicts of Interest: Venja Taube is an employee of BEST 3 Gefluegelernaehrung GmbH, Twistringen, Germany.
The BEST 3 Gefluegelernaehrung GmbH had no role in the design of the study; in the collection, analyses,
or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. Diana Siebert is
an employee of CJ Europe GmbH, Schwalbach, Germany. The CJ Europe GmbH had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.

References
1. De Vries, M.; de Boer, I.J.M. Comparing environmental impacts for livestock products: A review of life cycle
assessments. Livestig. Sci. 2010, 128, 1–11. [CrossRef]
2. Steinfeld, H.; Gerber, P.; Wassenaar, T.; Castel, V.; Rosales, M.; Rosales, M.; de Haan, C. Livestock’s Long
Shadow: Environmental Issues and Options; Food & Agriculture Org.: Rome, Italy, 2006.
3. Leip, A.; Billen, G.; Garnier, J.; Grizzetti, B.; Lassaletta, L.; Reis, S.; Simpson, D.; Sutton, M.A.; De Vries, W.;
Weiss, F. Impacts of european livestock production: Nitrogen, sulphur, phosphorus and greenhouse gas
emissions, land-use, water eutrophication and biodiversity. Environ. Res. Lett. 2015, 10, 115004. [CrossRef]
4. Meier, M.S.; Stoessel, F.; Jungbluth, N.; Juraske, R.; Schader, C.; Stolze, M. Environmental impacts of
organic and conventional agricultural products—Are the differences captured by life cycle assessment?
J. Environ. Manag. 2015, 149, 193–208. [CrossRef] [PubMed]
5. Ferket, P.R.; van Heugten, E.; van Kempen, T.A.T.G.; Angel, R. Nutritional strategies to reduce environmental
emissions from nonruminants. J. Anim. Sci. 2002, 80, E168–E182. [CrossRef]
6. Mallin, M.A.; Cahoon, L.B. Industrialized animal production—A major source of nutrient and microbial
pollution to aquatic ecosystems. Popul. Environ. 2003, 24, 369–385. [CrossRef]
7. Clark, M.; Tilman, D. Comparative analysis of environmental impacts of agricultural production systems,
agricultural input efficiency, and food choice. Environ. Res. Lett. 2017, 12, 064016. [CrossRef]
8. Leip, A.; Weiss, F.; Lesschen, J.; Westhoek, H. The nitrogen footprint of food products in the european union.
J. Agric. Sci. 2014, 152, 20–33. [CrossRef]

189
Sustainability 2018, 10, 3827

9. Ospina-Rojas, I.C.; Murakami, A.E.; Duarte, C.R.A.; Eyng, C.; Oliveira, C.A.L.; Janeiro, V. Valine, isoleucine,
arginine and glycine supplementation of low-protein diets for broiler chickens during the starter and grower
phases. Br. Poult. Sci. 2014, 55, 766–773. [CrossRef] [PubMed]
10. Blair, R.; Jacob, J.P.; Ibrahim, S.; Wang, P. A quantitative assessment of reduced protein diets and supplements
to improve nitrogen utilization. J. Appl. Poult. Res. 1999, 8, 25–47. [CrossRef]
11. Moran, E.T.; Bushong, R.D.; Bilgili, S.F. Reducing dietary crude protein for broilers while satisfying
amino-acid-requirements by least-cost formulation—Live performance, litter composition, and yield of
fast-food carcass cuts at 6 weeks. Poult. Sci. 1992, 71, 1687–1694. [CrossRef]
12. Bregendahl, K.; Sell, J.L.; Zimmerman, D.R. Effect of low-protein diets on growth performance and body
composition of broiler chicks. Poult. Sci. 2002, 81, 1156–1167. [CrossRef] [PubMed]
13. Laudadio, V.; Passantino, L.; Perillo, A.; Lopresti, G.; Passantino, A.; Khan, R.; Tufarelli, V. Productive
performance and histological features of intestinal mucosa of broiler chickens fed different dietary protein
levels. Poult. Sci. 2012, 91, 265–270. [CrossRef] [PubMed]
14. Laudadio, V.; Dambrosio, A.; Normanno, G.; Khan, R.U.; Naz, S.; Rowghani, E.; Tufarelli, V. Effect of reducing
dietary protein level on performance responses and some microbiological aspects of broiler chickens under
summer environmental conditions. Avian Biol. Res. 2012, 5, 88–92. [CrossRef]
15. Namroud, N.F.; Shivazad, M.; Zaghari, M. Effects of fortifying low crude protein diet with crystalline amino
acids on performance, blood ammonia level, and excreta characteristics of broiler chicks. Poult. Sci. 2008, 87,
2250–2258. [CrossRef] [PubMed]
16. Shao, D.; Shen, Y.R.; Zhao, X.; Wang, Q.; Hu, Y.; Shi, S.R.; Tong, H.B. Low-protein diets with balanced amino
acids reduce nitrogen excretion and foot pad dermatitis without affecting the growth performance and meat
quality of free-range yellow broilers. Ital. J. Anim. Sci. 2018, 17, 698–705. [CrossRef]
17. Khajali, F.; Wideman, R. Dietary arginine: Metabolic, environmental, immunological and physiological
interrelationships. World Poult. Sci. J. 2010, 66, 751–766. [CrossRef]
18. Wu, G.; Bazer, F.W.; Dai, Z.; Li, D.; Wang, J.; Wu, Z. Amino acid nutrition in animals: Protein synthesis and
beyond. Annu. Rev. Anim. Biosci. 2014, 2, 387–417. [CrossRef] [PubMed]
19. Council, N.R. Nutrient Requirements of Poultry; National Academic Press: Washington, DC, USA, 1994.
20. Corzo, A.; Kidd, M. Arginine needs of the chick and growing broiler. Int. J. Poult. Sci. 2003, 2, 379–382.
21. Corzo, A.; Moran, E., Jr.; Hoehler, D. Arginine need of heavy broiler males: Applying the ideal protein
concept. Poult. Sci. 2003, 82, 402–407. [CrossRef] [PubMed]
22. Siebert, D.; Khan, D.R.; Esteve-Garcia, E. Investigations on the optimal arginine:lysine ratio in the starter
phase of meat-type chickens. In Proceedings of the 21st European Society of Veterinary and Comparative Nutrition
Congress; Harris, P., Moore-Colyer, M., Eds.; European Society of Veterinary & Comparative Nutrition:
Cirencester, UK, 2017; Volume 21, p. 144.
23. Mayne, R.; Else, R.; Hocking, P. High litter moisture alone is sufficient to cause footpad dermatitis in growing
turkeys. Br. Poult. Sci. 2007, 48, 538–545. [CrossRef] [PubMed]
24. Slaoui, M.; Fiette, L. Histopathology procedures: From tissue sampling to histopathological evaluation.
In Drug Safety Evaluation; Springer: Cham, Switzerland, 2011; pp. 69–82.
25. Naumann, C.; Bassler, R. Methoden der Landwirtschaftlichen Forschungs-und Untersuchungsanstalt, Biochemische
Untersuchung von Futtermitteln; Methodenbuch iii (einschließlich der achten Ergänzungen); VDLUFA:
Darmstadt, Germany, 2012.
26. Aletor, V.A.; Hamid, I.I.; Niess, E.; Pfeffer, E. Low-protein amino acid-supplemented diets in broiler
chickens: Effects on performance, carcass characteristics, whole-body composition and efficiencies of
nutrient utilisation. J. Sci. Food. Agric. 2000, 80, 547–554. [CrossRef]
27. Ernährungsphysiologie, G.F. Empfehlungen zur Energie-und Nährstoffversorgung der Legehennen und Masthühner
(Broiler); DLG Verlag: Frankfurt am Main, Germany, 1999.
28. Kamran, Z.; Sarwar, M.; Nisa, M.; Nadeem, M.; Ahmad, S.; Mushtaq, T.; Ahmad, T.; Shahzad, M. Effect of
lowering dietary protein with constant energy to protein ratio on growth, body composition and nutrient
utilization of broiler chicks. Asian Austral J. Anim. 2008, 21, 1629–1634. [CrossRef]

190
Sustainability 2018, 10, 3827

29. Aviagen. Ross 308 Broiler Performance Objectives; Aviagen Group: Huntsville, AL, USA, 2014.
30. Willems, O.; Miller, S.; Wood, B. Aspects of selection for feed efficiency in meat producing poultry. World Poult.
Sci. J. 2013, 69, 77–88. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

191
 sustainability

Article
Production of Pig Feed under Future Atmospheric
CO2 Concentrations: Changes in Crop Content and
Chemical Composition, Land Use, Environmental
Impact, and Socio-Economic Consequences
Henrik Saxe 1, * ID
, Lorie Hamelin 2 , Torben Hinrichsen 3 and Henrik Wenzel 4
1 Mindful Food Solutions, Engbakkevej 3C, 2900 Charlottenlund, Denmark
2 Department of Engineering of Biological Systems and Processes (LISBP),
National Institute of Applied Sciences (INSA), INRA UMR792 and CNRS UMR5504,
Federal University of Toulouse, 135 Avenue de Rangueil, F-31077 Toulouse, France;
[email protected]
3 DSM Nutritional Products Ltd., Kirkebjerg Alle 88, 2605 Brøndby, Denmark; [email protected]
4 Institute of Chemical Engineering, Biotechnology and Environmental Technology,
SDU Life Cycle Engineering, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark;
[email protected]
* Correspondence: [email protected]; Tel.: +45-60742225

Received: 14 August 2018; Accepted: 2 September 2018; Published: 6 September 2018

Abstract: With the rising atmospheric CO2 , crops will assimilate more carbon. Yields will increase
in terms of carbohydrates while diluting the content of protein and minerals in compound pig
feed, calling for an altered formulation with more protein and less carbohydrate crops to maintain
its nutritional value. Using crop response data from CO2 exposures in a linear modeling of feed
formulation, we apply a consequential life cycle assessment (cLCA) to model all of the environmental
impacts and socio-economic consequences that altered crop yields and chemical composition at
elevated CO2 levels have on feed formulation, targeting altered amino acid contents rather than
overall protein. An atmospheric CO2 of 550 μmole mole−1 gives rise to a 6% smaller demand for
land use for pig feed production. However, feed produced at this CO2 must include 23% more
soymeal and 5% less wheat than at present in order to keep its nutritional value. This counteracts the
yield benefit. The monetized environmental cost of producing pig feed, where sunflower and soy
contribute the most, equals the direct feed price in both scenarios. If external costs were internalized,
honoring the Rio Declaration, feed prices would double. In contrast, the future composition of pig
feed will increase the direct price by only 0.8%, while the external cost decreases by only 0.3%.

Keywords: amino acids; compound pig feed formulation; consequential life cycle assessment; cLCA;
land-use changes (LUC); monetized environmental impact; protein crops; starch (energy) crops

1. Introduction
During this century, the rising atmospheric carbon dioxide concentration (CO2 ) is expected to
increase crop yields due to increased carbon assimilation, for example in wheat grains, by 10% [1].
On the other hand, the higher carbon uptake causes increased starch content, and consequently also a
dilution of the relative protein and mineral content in food and feed crops [2]. Additional consequences
of future atmospheric CO2 include altered patterns of temperature and precipitation, which together
with regional changes, e.g., ozone pollution and nitrogen (N) fertilization, will further modify plant
growth and its chemical composition.

Sustainability 2018, 10, 3184; doi:10.3390/su10093184 192 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3184

The animal feed market, which currently absorbs approximately 45%, 58%, and 80% of the
world cereal, maize, and soy, respectively [3], is likely to be affected by such changes in crop yield
and composition. In fact, since the composition of animal feed for intensive livestock production is
carefully optimized in order to meet both the applying legislation and the nutritional requirements in
a cost-effective manner, any change in both the chemical composition and the yield of feed crops will
affect the future formulation of the feed.
Although the environmental consequences of the forecasted future increases in meat (and thus feed)
demand have been overly studied (e.g., references [4–6]), there are no studies, to the authors’ knowledge,
that have attempted to address the environmental impacts related to the changes that a higher CO2
would induce to the feed market. From an environmental perspective, a (CO2 -induced) higher crop
yield would contribute to reduce both the land use and the land-use changes that are associated with
increased demand for animal feed. On the other hand, lower protein content would trigger an increased
need for protein-rich crops such as soybeans, which in turns would involve an increased land-use
change, the environmental impact of which may be considerable (e.g., references [7–9]). Yet, it is not
clear which effect would dominate over the other. Further, a change in protein content has to be
addressed with regards to the specific amino acids affected, as a change in some non-essential amino
acids (e.g., proline) is rather useless for the overall feed composition.
Focusing on the effects of elevated CO2 alone, this study endeavors to assess the environmental
consequences, the associated environmental cost, and the direct price of compound pig feed based
on the yield and chemical composition of crops grown at the “present” atmospheric CO2 (taken at
380 μmole CO2 mole−1 dry air) and at a “future” CO2 (550 μmole mole−1 dry air by 2050 [10]).
From this point onwards, the former will be referred to as “present feed”, and the latter will be
referred to as “future feed”, with the understanding that these are both compound feeds. Further,
the socio-economic consequences are, in this study, represented by the sum of the direct price and the
cost of environmental impacts (so-called shadow price) of producing compound pig feed. Compound
feed means multi-component animal feed produced at a competitive price to satisfy all of the nutritional
and technical needs in terms of carbohydrates, protein, oils, fiber, enzymes, vitamins, etc.

2. Materials and Methods

2.1. Life Cycle Assessment (LCA) Model

Consequential life cycle assessment (cLCA, e.g., references [11,12]) modeling was used to assess
the environmental burdens of producing one extra tonne (the functional unit) of pig feed produced
today (present CO2 scenario) and in a future with 550 μmole CO2 mole−1 (future CO2 scenario).
The life cycle impact assessment was carried out using the stepwise method, which allows
for the full monetarization of environmental impacts (expressed in €2003). This method combines
characterization models from IMPACT2002 + v2.1 and EDIP2003 and is further described in
reference [13]. The assessment was facilitated with the LCA software Simapro® 7.3.3. Translating all
of the environmental impact into monetized costs enables the selection and presentation of the most
important environmental impact categories causing the socio-economic impacts of compound pig
feed (other impact categories are presented in Supplementary). Biogenic carbon (C), including soil C
changes and C sequestration by feed crops, was included in all of the calculations in order to allow for
a transparent carbon balance, as described by reference [14].
Background LCA data were taken from the Ecoinvent v.2.2 database [15], while foreground data
were essentially related to the cultivation, yield, and chemical composition of the crops used in feed
formulation. These are described in Section 2.4 and Supplementary. The geographical scope considered
for the foreground system was Denmark, i.e., the pig feed was considered to be manufactured for the
Danish market. The Danish example is taken as representative for most industrialized countries in a
temperate climate.

193
Sustainability 2018, 10, 3184

2.2. LCA System Boundary

All of the processes affected by the production of one tonne of pig feed, i.e., from crop cultivation
to harvest, and up to the mixing of the feed, were included within the LCA system boundary. Direct as
well as indirect land-use changes were also included in the study (Section 2.4). As the focus of
the study is on the production of the feed itself, processes downstream from the feed production
(e.g., consumption by the animals) were excluded, as these were outside of the study’s scope.
Based on the cLCA principles, system expansion was performed for all of the feed ingredients
affected by the considered change of atmospheric CO2 .

2.3. Feed Formulation and Life Cycle Inventory (LCI)

2.3.1. Formulation of Present and Future Pig Feed

To apply a market-based approach, the commercial feed formulation software Bestmix® [16]
was used to establish both the present and future feed formulation for piglets, sows, and slaughter
pigs (a feed mix consisting of 20% piglet feed, 20% sow feed, and 60% fattening pig feed was
considered, because this is what is used in a normal pig life cycle). Through optimization algorithms,
Bestmix® formulated the best compromise between profitability, nutritional value, and animal health,
while ensuring that the Danish and European legal requirements of the feed were met. This procedure
allowed determining the exact ingredient proportions constituting the present and future pig feed.
One important input to Bestmix® is the chemical composition of crop ingredients, in terms of
starch, protein, amino acids, macronutrients, and micronutrients. Another important input parameter
to Bestmix® is the price of feed ingredients. However, as the aim of this study is primarily to investigate
the consequences of altered crop composition, and since no reliable estimate is available on future
crop prices, the prices of crop ingredients under a high CO2 future were taken to be equal to the
present prices.
The chemical composition of all of the crop ingredients, when grown under today’s atmospheric
CO2 , was established based on the Danish Pig Research Centre feed ingredients database [17]. Data on
the yield and chemical composition of the crop ingredients grown at 550 μmole CO2 mole−1 was
established based on data from growth experiments with increased CO2 exposure taken from the
scientific literature. Reliable data was only found for the four main crop ingredients (Table 1):
namely wheat, barley, soy, and rape, which together make up 89% of the present pig feed by dry
weight (Table 2).
Since there is a large variability reported in the literature for plant responses to elevated CO2 ,
the following principles for selection of the best data were adopted. Results from Free Air Carbon
Dioxide Exposure (FACE) systems were assumed to provide the most reliable data, since they represent
the most realistic growing conditions, although FACE responses are typically smaller than for other
exposure systems, see e.g., references [18,19]. When FACE data were not available, data from open-top
chambers (OTC), from outdoor closed-top chambers (CTC), or from climate chambers were used,
in that order of ranking. As crops respond differently to elevated atmospheric CO2 with different
climatic or other abiotic or biotic conditions, exposure experiments that were performed near to
where the feed ingredients that were considered in this study were grown were preferred over other
studies. Even with the same exposure technique, all of the studies give different results for each year,
and with each plant species, it varies with the studied cultivar. Under these conditions, either the
best available reference was applied for each species and chemical component, or data from meta
studies were applied. When data for future chemical content was not found for a given component
(e.g., amino acids), the future content was presumed to be the same as today. The chosen data sources
are summarized in Table 1.

194
Sustainability 2018, 10, 3184

2.3.2. Life Cycle Inventory (LCI) Data for Crop and Non-Crop Ingredients

Crop Ingredients
The LCI of crops grown in Denmark (wheat and barley) was based on a recent Danish
consequential LCI dataset [14], which comprises all of the processes involved during the cultivation
stage, up to harvest. This includes the tillage activities, liming, seed propagation, plant protection,
fertilization, sowing, harvest, and transport from farm to field. A sandy soil has been considered
for both crops, as well as precipitations of 964 mm y−1 and removal (harvest) of the straw. LCI data
from the Ecoinvent (v.2.2) database were used to model the cultivation of imported soybean (Brazil),
rapeseed (Germany), sunflower (Spain), and palm oil (Malaysia). Other important foreground data for
crop ingredients are thoroughly described in the appendices.

Industrial Amino Acids

As shown in Table 2, two types of industrial amino acids are included in the assessed pig feed:
industrial amino acids produced by fermentation (lysine, threonine, and tryptophan) and industrial
amino acids produced synthetically (dl-methionine). Based on reference [19], a generic recipe was
considered for 1 kg of amino acids produced by fermentation; 1 kg of sugar (from sugar beet), 0.5 kg
of maize starch, 0.5 kg of wheat starch, 0.3 kg of liquid ammonia, and 36 MJ of process energy at
the plant. In this study, the recipe was supplemented with 0.053 kg of sulfuric acid per kg amino
acid, and 4.6 g of phosphorous based on data from the Danish lysine supplier (see Supplementary).
Under Danish production conditions, the energy consumption was estimated at only 18 MJ, which was
supplied as electricity (50%) and natural gas (50%). On the basis of reference [20], it was assumed that
the production of 1 kg of dl-methionine required 0.43 kg of propylene, 0.27 kg of hydrogen sulfide,
0.39 kg of methanol, 0.21 kg of hydrogen cyanide, and 7.4 MJ of process energy at the plant, which was
supplied by electricity (50%) and natural gas (50%).

Enzymes
No specific LCI data were found for the added enzymes (phytase, xylanase). Instead, published
LCA data for phytase (i.e., characterization results for global warming, acidification, nutrient
enrichment, photochemical ozone formation, land use, phosphorus consumption, and energy
consumption) were used for both types of enzymes [21].

Other Ingredients
In the absence of LCI data for the vitamins added to the compound pig feed, these ingredients
were calculated as for enzymes. LCI data for limestone meal (CaCO3 ), monocalcium phosphate (MCP),
phosphoric acid, and sodium chloride (NaCl) were taken from the Ecoinvent (v.2.2) database. LCI data
for fish meal were taken from the LCA food database (“industrial fish, ex harbor”, as available in
Simapro 7.3.3).

2.4. Land-Use Changes (LUC)

In order to quantify the environmental consequences of land-use changes, three main steps
are required: (i) determining the total land area undergoing conversion to cropland; (ii) identifying
which land types (i.e., biomes) are converted; and (iii) determining the changes in carbon flows from
these conversions. Direct and indirect land-use change (LUC) have been extensively studied over
the past decade for all of the major global ecosystems [8,22–25]. LUC also impacts biogeochemical
cycling [26,27] and biodiversity [28], but these aspects have not yet been sufficiently quantified, and can
therefore not be included in the present analyses.

195
Sustainability 2018, 10, 3184

2.4.1. Land Conversion: Determination of the Area and Geographical Location (Steps i and ii)
In this study, a deterministic explorative approach based on crop yields (Table 1), carbohydrate
content, lysine content, and historical market trends has been used in order to determine the
above-mentioned steps (i) and (ii). This is further described below. As a starting point, the LUC
involved in this study may be classified in two distinct categories: (a) those triggered by the
displacement of carbohydrates crops, and (b) those triggered by the displacement of oil crops.
The former represents the LUC resulting from the cultivation of crops whose increased demand
(as a result of producing one extra tonne of Danish pig feed) involves the displacement of a
carbohydrate crop. This can be illustrated by the case of wheat (Figure 1). As shown in Figure 1,
an extra demand of one tonne of Danish pig feed induces a need for an additional 480 kg of wheat
(present feed) and 460 kg of wheat (future scenario). These figures were determined from Bestmix®
data, as presented in Table 2.

(a)

(b)

Figure 1. Consequential life cycle assessment (LCA) model for wheat grown (a) at the present CO2 and
(b) at the future CO2 . Dotted lines indicate avoided flows. All of the flows are related to the functional
unit, i.e., 1 tonne of compound Danish pig feed.

In a country such as Denmark, where 65% of the total land is used for cropland, and where policies
have been adopted in order to double the forested area (nowadays representing ca. 13% of the total
land [29]), very limited conversion from forest or similar nature types is realistic. Most likely, the land
that is needed to grow this extra wheat will be taken from actual Danish cropland, which means that
one crop cultivated today will be displaced. Such a displaced crop is, in cLCA, referred to as the
marginal crop. In this study, the marginal crop was assumed to be spring barley (a carbohydrate
crop), based on references [30,31]. The environmental consequences of cultivating wheat instead of
spring barley represent, in this case, the so-called direct land-use changes (dLUC). Indirect land-use
changes (ILUC), on the other hand, represent the environmental consequences that are related to how
this missing supply of Danish spring barley will be supplied on the world market. Such increased
crop production may stem from increased yield, which is also referred to as intensification, or from
land conversion to cropland, which is also referred to as agricultural land expansion. As illustrated
in Figure 1, and as in many ILUC or LCA studies (e.g., references [32–35]), this study includes the
environmental impacts of the latter only.

196
Sustainability 2018, 10, 3184

Similar to wheat, an increased demand for land in Europe in order to cultivate the barley, rapeseed
meal, and sunflower meal (Table 2) resulting from an extra demand of Danish pig feed was considered
to take place at the expense of spring barley. The process flow diagrams for these crops are illustrated
in Supplementary.
An extra demand for soybean meal, rapeseed meal, sunflower meal, and palm oil also implies
an interaction with the vegetable oil market (category “b” above). For the latter, this interaction is
straightforward. For the three former, the interaction is indirect and happens as oil is co-produced with
the desired meal. This can be illustrated with the case of soybean meal (Figure S3 in Supplementary).
Increased soybean meal production involves increased soy oil co-production, causing a decrease in
palm oil production (palm oil being identified as the marginal oil, on the basis of the references [30,31]),
and consequently also a decrease in the co-produced palm meal (a source of both protein and
carbohydrates), inducing, somewhere in the world, an increase in the production of a marginal
protein and carbohydrate feed crop. Since the production of a marginal protein interacts with
the oil market again, a loop system is thus created, and this loop should be stopped at the point
where the consequences are so small (or the uncertainties so large) that any further expansion of the
boundaries would yield no significant information for decision support [36]. Such flows are illustrated
in Supplementary for all of the crops interacting with the oil market. A substitution ratio of 1:1 was
assumed, i.e., that 1 t of a given vegetable oil would replace 1 t of the marginal oil (palm oil), since it is
the long-term effect of the demand that should be guiding for decisions in LCA [37]. In other words,
the supply of goods and services was assumed to be fully elastic, and accordingly, short-term effects
are not captured.
For LCA models of soy, rape, and sunflower that all involve the displacement of palm meal
as a result of the above-described oil loop, soybean meal was identified as the reacting marginal
protein [30,31]. Being the market covering the greatest share of the worldwide increase in soybean
production [38], soybean from South America (Argentina and Brazil) was identified as the market
reacting to an extra demand for soybean meal. Based on a similar logic, palm fruit cultivation from
Southeast Asia was identified as the one reacting to an extra demand.
When applying a deterministic approach to land-use changes in LCAs, it has been a common
practice to determine the amount of marginal protein crop (here soybean meal) reacting to a decrease
in palm meal production on the basis of the protein content of these meals, e.g., references [23,31,39].
However, it is the composition of the protein in terms of amino acids, or rather in terms of the limiting
amino acids, that matters for feed. The most important limiting amino acid in pig feed is lysine.
Therefore, the reacting amount of soybean meal has been identified on the basis of the lysine content
of the meals (Supplementary).
For fermentation-based amino acids, which are produced from of a mix of different crops
(Supplementary), the same principles as described above were applied. For each crop system, all of
the details of the inventory data that were used for determining the area and geographical location
of the land converted are presented in Supplementary. Further, it has been considered, on the basis
of reference [34], that only 80% of the new soy and carbohydrates demand is supplied through
land expansion, while this was 70% for palm oil. The remaining production must be supplied by
the intensification of existing areas (the various types of intensification pathways and the extent
to which each is driven by crop prices is discussed in reference [40]. As previously highlighted,
the environmental impacts of such intensification were not included in this study. With input-driven
intensification, the reduced environmental impact associated with increased crop yield is countered by
the environmental impact of an increased use of fertilizers, pesticides, and machinery, among others.

2.4.2. Environmental Consequences of Land Conversion

The dLUC consequences, in terms of changed C and N flows, of cultivating a given crop in Europe
instead of spring barley have been included and modeled on the basis of the data from reference [14].

197
Sustainability 2018, 10, 3184

In order to quantify the releases of carbon due to the land converted to cultivate soybean,
palm fruit, or the reacting carbohydrate mix, the soil and vegetation carbon data from the Woods Hole
Research Centre, as published in reference [8], was used. This allowed the calculation of the CO2
emitted during land conversion (i.e., step (iii) referred to in the first sentence of Section 2.4), where the
following has been considered:

• 25% of the carbon in the soil is released as CO2 for all types of land-use conversion, except when
forests are converted to grassland, where 0% is released;
• 100% of the carbon in vegetation is released as CO2 for all of the forest types as well as for tropical
grassland conversions, while 0% is released for the remaining biome types (e.g., shrub land,
non-tropical grassland, chaparral).

The results of this calculation are shown in Supplementary; flows were annualized (distributed
equally) over 20 years, which is in line with most LUC calculations used by European policy makers [41].
A similar procedure has also been applied by reference [35].

2.5. Direct Cost

Based on today’s market prices for all of the ingredients (as available in Bestmix® ), the price of
one tonne compound pig feed for the present and future atmospheric CO2 were calculated.

3. Results and Discussion

3.1. Changes in Crops’ Chemical Composition and in the Compound Feed Formulation
Table 1 shows the established present and future chemical composition of wheat, barley, soymeal,
and rape meal used as input to Bestmix® [16]. The optimization performed in Bestmix® determined
that one tonne of compound pig feed produced under the future relative to the present atmospheric
CO2 will contain 5.1% less wheat, 23% more soy, unchanged amounts of barley, rape, and sunflower,
18% more beet molasses, 65% more hemoglobin meal, 16% less amino acids produced by fermentation
(lysine, threonine, tryptophan), and varying amounts of other minor ingredients (Table 2). The results in
Table 2 thus support the hypothesis that pig feed based on wheat, barley, and rape grown in Northern
Europe under higher CO2 will need a higher supplement of protein as well as less carbohydrate
ingredients. Table 2 also highlights that both present and future feed consist of at least 46% wheat,
25% barley, 9% soy meal, 7% rape meal, and 4% sunflower seeds; these five ingredients making up
approximately 93% of the feed.

3.2. Environmental Impact

Characterized LCA results are presented in Figure 2, with a focus on the four socio-economically
most important impact categories, which were identified through normalization (Section 3.4);
human toxicity in terms of non-carcinogenic organics and respiratory inorganics (PM2.5 );
nature occupation; and global warming. The results for all of the other evaluated impact categories are
given in Supplementary (Figures S8 and S9).
The environmental impact of producing one extra tonne of compound pig feed was expected
to decrease in the high CO2 future due to the higher yields (and thus lower land use) caused by the
higher CO2 uptake from the atmosphere. However, even though the yield increases were found to
be large, e.g., 10% for wheat and 28% for rape, the net land use did not decrease to the same extent.
The net reduction in land use per tonne of pig feed was found to be around 6%. Unexpectedly, this did
not lead to a net fall in greenhouse gas emissions per tonne of feed; on the contrary, it increased by 9%
for crops grown at the future CO2 (explained in detail in Supplementary, Figure S10). This is essentially
due to the change in feed composition, where considerably more soybean meal, which involves the
conversion of biomes with relatively high C stock, is required under a high CO2 . This is reflected in
Table 2 and Figure 2.

198
Sustainability 2018, 10, 3184

However, the biggest differences are found for the impact categories of respiratory inorganics
(fine particles) and non-carcinogenic human toxicity (17% increase and 18% decrease, respectively).
Again, these differences between the present and future CO2 scenarios can be explained by the change
in the feed’s chemical composition, especially the increased need for soy meal and decreased need for
wheat at elevated atmospheric CO2 .
Nearly all of the impacts are due to the crop-based ingredients, i.e., the sum of others (non-crop
ingredients) is infinitesimal (reflected in Figure 3 discussed in Section 3.4). For non-carcinogenic human
toxicity, rape and wheat are the biggest contributors (caused by rape and wheat cultivation, but the
effect of wheat will be greatly reduced by the displaced barley; Figure 1). For respiratory inorganics,
soy and wheat are the major contributors (caused by soy and wheat cultivation, but the effect of wheat
will be greatly reduced by the displaced barley, and that of soy will be somewhat reduced by soy oil
displacing palm oil; see Figure S3 in Supplementary), while rape contributes negatively (mainly due
to displaced palm oil; Figure S4). Regarding natural occupation, all of the main crop ingredients
contribute, and sunflower the most (due to the low yield of sunflower cultivation and the displaced
barley; Figure S5). For global warming, soy is the biggest overall contributor (71% of its contribution
is caused by indirect land-use change, 19% by soy oil displacing palm oil; Figure S3), followed by
barley. These observations emphasize that each crop ingredient in compound pig feed contributes
differently to the various environmental impacts of the feed based on their content, and that ILUC
is important in the calculation of the overall GWP (Global Warming Potential) of feed production,
second only to crop and displaced crop cultivation. Cultivation of the main crops (photosynthetic
carbon uptake) as well as the reacting carbohydrate crop cultivation all contribute negatively to the
GWP impact (Supplementary, Figure S10).
WRQQHRIFRPSRXQGSLJIHHGDWWKHIXWXUH&2
5HODWLYHHQYLURQPHQWDOLPSDFWRIFURSVLQRQH

100 % (0.39)


FRQFHQWUDWLRQUHODWLYHWRWKHSUHVHQW

100 % (45.8)

117 %

100 % (1117)

100 % (613)


109 %
82 %

94 %


x 
x  x  x  x 
 ͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲͲ x  x 
x  
    





ƉƌĞƐĞŶƚ΀KϮ ΁


 ĨƵƚƵƌĞ΀KϮ ΁







 ƉƌĞƐĞŶƚ΀KϮ ΁

 ĨƵƚƵƌĞ΀KϮ ΁







 ƉƌĞƐĞŶƚ΀K ΁

EĂƚƵƌĞŽĐĐƵƉĂƚŝŽŶ;ŵ ĂŐƌŝĐ͘ůĂŶĚͿ ĨƵƚƵƌĞ΀K ΁







 ƉƌĞƐĞŶƚ΀K ΁


΁


Ϯ

ĨƵƚƵƌĞ΀KϮ

$$IHUPHQW
%DUOH\
3DOPRLO


















EŽŶͲĐĂƌĐ͘ŚƵŵĂŶƚŽdžŝĐŝƚLJ;ŬŐϮ,ϯůͲĞƋͿ

ZĞƐƉŝƌĂƚŽƌLJŝŶŽƌŐĂŶŝĐƐ;ŬŐWDϮ͘ϱͲĞƋͿ

'ůŽďĂůǁĂƌŵŝŶŐ;ŬŐKϮͲĞƋͿ



5DSH
6R\
6XQIORZHU
:KHDW
6XPRIRWKHUV
Ϯ

 ,PSDFWFDWHJRULHV

Figure 2. Relative environmental impacts of producing one tonne of compound pig feed under future
and current CO2 for the socio-economically four most important impact categories. The dots represent
the net value of the environmental impact, i.e., the positive minus the negative values. Eq: equivalents;
PM2.5 : ultrafine particles; AA ferment.: amino acids produced for feed by fermentation processes
(lysine, threonine, tryptophan).

199
 Sustainability 2018, 10, 3184

Table 1. Chemical composition and yield of wheat, barley, soy, and rape at the present (380 μmole mole−1 ) and future (550 μmole mole−1 ) atmospheric
CO2 concentrations.

Wheat, Denmark Barley, Denmark Soy, Argentina/Brazil Rapeseed, Germany

Chemical Composition
Present 1 Change 2 (%) Future 7 Present 1 Change 3, 4 (%) Future Present Change 3 (%) Future Present 1 Change 5 (%) Future
Total Dry Matter, % 85 0 85 85 0 85 88 unknown unknown 89 unknown unknown
Starch (g/kg) 670 +7.5 720 630 +4.1 4 660 27 unknown unknown 19 unknown unknown
Raw Protein, % 9.5 −14 8.2 9.7 −15 3 8.2 47 −1.4 46 35 −4.6 33
Amino Acids (g/kg)
Lysine 2.3 −10 2.0 2.6 unknown unknown 26 unknown unknown 15 −2.5 14
Methionine 1.3 −17 1.1 1.4 unknown unknown 5.7 unknown unknown 6.0 −4.3 5.7
Cystine 1.9 −17 1.6 1.8 unknown unknown 5.8 unknown unknown 7.0 −5.4 6.6
Threonine 2.2 −21 1.8 2.4 unknown unknown 16 unknown unknown 12 −1.8 11
Tryptophan 0.93 −17 0.77 0.93 unknown unknown 5.7 unknown unknown 3.3 −3.1 3.2
Isoleucine 2.8 −22 2.2 2.7 unknown unknown 18 unknown unknown 11 −3.1 10
Leucine 5.2 −19 4.2 5.1 unknown unknown 32 unknown unknown 20 −3.7 19
Histidine 1.9 −16 1.6 1.7 unknown unknown 11 unknown unknown 8.1 −3.9 7.7
Phenylalanine 3.6 −14 3.1 3.7 unknown unknown 21 unknown unknown 11 −1.9 11
Tyrosine 2.4 −16 2.0 2.3 unknown unknown 16 unknown unknown 8.2 −2.6 8.0
Valine 3.5 −8 3.2 3.6 unknown unknown 20 unknown unknown 14 −3.4 13

200
Macroelements (g/kg) (4)

Calcium 0.43 −15 0.36 0.43 4.8 0.45 3.5 unknown unknown 8.5 −1.5 8.4
Phosphorus 2.6 −4 2.5 3.0 −4.6 2.8 6.8 unknown unknown 11 1.8 11
Sodium 0.085 −6 0.080 0.17 unknown unknown 0.18 unknown unknown 0.36 0.1 0.36
Potassium 5.0 −1 4.9 4.8 0 4.8 22 unknown unknown 13 0.3 13
Magnesium 1.0 −7 0.95 1.0 −3.3 0.99 3.2 unknown unknown 4.7 0.8 4.8
Sulphur 1.1 −13 0.96 0.94 −5.0 0.89 3.6 unknown unknown 6.5 −6.1 6.1
Microelements (mg/kg) (4)

Iron 27 −18 22 29 −11 26 260 unknown unknown 230 1.0 230

Manganese 25 −3 24 12 unknown unknown 47 unknown unknown 68 −2.6 66
Zink 34 −13 30 24 −13 21 48 unknown unknown 65 −5.6 61
Yield (t fm ha−1 ) 6.8 6 +11% 5 7.3 5.0 6 +20% 8 6.0 3.4 9 +15% 10 3.9 3.8 11 + 5.0% 12 4.0
1:reference [17]; 2 : Based on OTC data in reference [19]; 3 : reference [42], meta-data; 4 : reference [43], FACE data; 5 : reference [44], FACE data, extrapolation assuming linear responses to
elevated CO2 , 6 : reference [14]; 7 : reference [1], FACE data, extrapolation assuming linear responses to elevated [CO2 ]; 8 : reference [45], OTC data; 9 : reference [31]; 10 : reference [46],
FACE data; 11 : reference [38], average 2005–2010; 12 : reference [47], RERAF chamber data.
 Sustainability 2018, 10, 3184

Table 2. Ingredients in Danish pig feed for piglets, sows, and slaughter pigs, and their weighted average, produced at the present (380 μmole mole−1 ) and
future (550 μmole mole−1 ) atmospheric CO2 concentrations. Amino acids produced by fermentation include lysine, threonine, and tryptophan. Dl-methionine is
chemically synthesized.

Product Main Function in the Feed Sow Feed (20%) Piglet Feed (20%) Slaughter Pig Feed (60%) Weighted Average Pig Feed
Present Future Present Future Present Future Present Future Absolute Change Relative Change
Percent by Mass (Dry Weight Basis) kg percent
Wheat Energy 52 50 46 44 47 45 48 46 −25 −5.1%
Barley Energy 25 25 25 25 25 25 25 25 0.0 0.0%
Soy meal Protein 6.0 8.6 19 20 6.9 9.4 9.2 11 +22 +23%
Rape meal Protein 4.0 4.0 0.0 0.0 10 10 6.8 6.8 0.0 0.0%
Sunflower meal Protein 6.0 6.0 0.0 0.0 5.0 5.0 4.2 4.2 0.0 0.0%
Beet molasses Energy 2.0 2.0 0.50 2.0 2.0 2.0 1.7 2.0 +3.0 +18%
PFAD oil, palm fatty acid distillate Energy and technical aid 1.3 1.3 1.5 1.3 1.3 1.3 1.3 1.30 −0.39 −2.9%
Limestone meal (CaCO3 ) Production requirement 1.4 1.3 0.86 0.85 1.3 1.3 1.2 1.2 −0.25 −2.1%
Amino acids (fermentation) Production requirement 0.37 0.28 0.73 0.66 0.48 0.40 0.51 0.43 −0.81 −16%
Salt, sodium chloride: Production requirement 0.43 0.42 0.46 0.50 0.50 0.44 0.48 0.45 +0.02 +6.3%
Monocalcium phosphate: Production requirement 0.64 0.66 0.88 0.94 0.22 0.23 0.43 0.47 +0.34 +5.5%
Protein (from fish): Protein 0.00 0.00 2.00 2.00 0.00 0.00 0.40 0.40 0.00 0.0%
Vitamins Production requirement 0.59 0.59 0.20 0.20 0.20 0.20 0.32 0.32 0.00 0.0%
Phytase and xylanase Health, economy, environment 0.04 0.04 0.14 0.14 0.08 0.08 0.08 0.08 0.00 0.0%
Dl-methionine (synthetic) Production requirement 0.00 0.00 0.10 0.11 0.00 0.01 0.02 0.03 +0.03 +14%

201
Hemoglobin meal Protein 0.00 0.00 1.00 1.7 0.00 0.00 0.20 0.34 +1.4 +65%
Formic acid, calcium salt PH-adjustment 0.00 0.00 0.80 0.80 0.00 0.00 0.16 0.16 0.00 0.0%
Sum 100 100 100 100 100 100 100 100
Note: PFAD—Palm Fatty Acid Distillates.
Sustainability 2018, 10, 3184

Amino acids produced by fermentation contribute negatively to each of the main impact categories.
This is because sugar production (one of the substrates in the fermentation process producing amino
acids) gives rise to by-products (molasses and pulp), which can substitute the use of marginal
carbohydrates for animal feed. The saved carbohydrates production (and the land-use changes
it generated) had a greater negative impact than the positive impact from the consumed sugar
substrate (see Figure S7a in Supplementary). Yet, these effects are of course highly dependent upon
the data quality that is used to model them. As three crop ingredients are used to produce these
amino acids (Figure S7a–c in Supplementary), and as each of these crops involve at least three
co-products, a considerable degree of uncertainty is introduced in the model, as a result of the
numerous assumptions involved regarding the displacement effects (i.e., system expansion).

3.3. Direct Cost

Data for direct market prices of all of the ingredients were added up for each pig growth stage
(Table 3). Based on the present prices of commodities and the altered content of future feed, an increase
in the direct costs for future pig feed was estimated at €1.92 per tonne of pig feed, which represents an
increase of only 0.8% on top of the current price of €250.39 per tonne.

Table 3. Differences in direct costs for present and future compound pig feed, on the basis of
today’s prices.

Present CO2 Future CO2 Difference

Sows, 200 kg feed €47.69 €48.14 €0.45
Piglets, 200 kg feed €60.92 €61.05 €0.13
Slaughter pigs, 600 kg feed €141.78 €143.12 €1.34
Total pig feed, 1000 kg €250.39 €252.31 €1.92
Per cent 100% 100.77% 0.77%

These results indicate that the direct price of future pig feed will not increase significantly due
to elevated atmospheric CO2 . However, it may, very well increase due to other circumstances, e.g.,
increasing prices on land, energy, fertilizers and pesticides, transport, manufacture, and increased
demand. If the demand for protein in animal feed continues to rise, the price of soy is likely to go up,
and soy in European pig feed may be replaced with other protein sources combined with an increased
application of industrial amino acids. However, all of these circumstances are impossible to foresee in
any detail, and are not directly related to the rising atmospheric CO2 .

3.4. External Environmental Cost

In the future, the external cost that is associated with the environmental impact of growing crops
may be included in the actual cost of food and feed according to “the polluter pays principle” [40],
significantly increasing the current price for compound pig feed. This in itself makes calculations of
external cost of pig feed production relevant.
Figure 3 shows the monetized environmental impact using the stepwise normalization
methodology [13] for the four most important impact categories, and the sum of 12 other categories.
As indicated in Figure 3 (and further detailed in Figure S11 and S12 in Supplementary), the cost of
the overall environmental externalities of one tonne of pig feed is estimated at €236.05 for the present
CO2 , and at €235.26 for the future CO2 , i.e., €0.79 or 0.3% less than feed produced today. These results
indicate that elevated CO2 will not increase the external environmental costs of pig feed.
As highlighted in Table 3 and Figure 3, the external socio-economic costs of producing compound
pig feed are in the same order of magnitude as the direct costs of pig feed. In fact, internalizing the
environmental externalities of producing pig feed nearly doubles the present (direct) cost of pig feed,
which is a vast price increase if the Rio Declaration is to be taken seriously [48].

202
Sustainability 2018, 10, 3184



€ 138.60
dŽƚĂůĞŶǀŝƌŽŶŵĞŶƚĂůĐŽƐƚŽĨ $$IHUPHQW

0RQHWL]HGHQYLURQPHQWDOLPSDFW¼

€ 130,48
ϭƚŽŶĞdžƚƌĂĐŽŵƉůĞƚĞƉŝŐĨĞĞĚ͗ %DUOH\
ƚƚŚĞƉƌĞƐĞŶƚ΀KϮ΁сϮϯϲ͘ϬϱΦ 3DOPRLO
5DSH
 ƚƚŚĞĨƵƚƵƌĞ΀KϮ΁сϮϯϱ͘ϮϲΦ
6R\
Ϭ͘ϳϵΦŽƌϬ͘ϯйůĞƐƐŝŶƚŚĞĨƵƚƵƌĞ
6XQIORZHU


:KHDW
VXPRIRWKHUV



€ 55.69
€ 50.89
€ 30.86
€ 26.27

€ 12.42


€ 10.21

€ 8.45
€ 8.30




 


ƉƌĞƐĞŶƚ΀KϮ ΁


ĨƵƚƵƌĞ΀KϮ ΁






ƉƌĞƐĞŶƚ΀KϮ ΁


ĨƵƚƵƌĞ΀KϮ ΁





ƉƌĞƐĞŶƚ΀KϮ ΁


ĨƵƚƵƌĞ΀KϮ ΁






ƉƌĞƐĞŶƚ΀KϮ ΁


ĨƵƚƵƌĞ΀KϮ ΁


ƉƌĞƐĞŶƚ΀KϮ ΁


ĨƵƚƵƌĞ΀KϮ ΁







ZĞƐƉŝƌĂƚŽƌLJŝŶŽƌŐĂŶŝĐƐ;ŬŐWDϮ͘ϱͲĞƋͿ













EĂƚƵƌĞŽĐĐƵƉĂ͘;ŵ ĂŐƌŝĐ͘>ĂŶĚͿ






'ůŽďĂůǁĂƌŵŝŶŐ;ŬŐKϮ ͲĞƋͿ





^ƵŵŽĨƌĞŵĂŝŶŝŶŐŝŵƉĂĐƚĐĂƚĞŐŽƌŝĞƐ
EŽŶͲĐĂƌĐ͘ŚƵŵ͘ƚŽdž͘;ŬŐϮ,ϯůͲĞƋͿ


Ϯ

,PSDFWFDWHJRULHV

Figure 3. Breakdown of the monetized environmental impact results per ingredient. The white dots
represent the net value of the environmental impact, i.e., the positive minus the negative values.
Eq: equivalents; PM2.5 : ultrafine particles; AA ferment.: amino acids produced by fermentation
(lysine, threonine, tryptophan).

Figure 3 (as Figure 2 and the extended Figures S9–S12 in Supplementary) highlights soy as a main
contributor to most of the environmental impact categories, whereas for natural occupation, sunflower
is the major contributor. Figure 3 also highlights the important contribution of the natural occupation
category, when environmental impacts are translated into a common monetized environmental impact,
which explains why the overall high environmental cost of sunflower is associated with a low yield.
Per tonne of pig feed, soy has the largest environmental impact in monetary terms, followed by
sunflower (Table 4). However, relative to their content in pig feed, sunflower has an 11-times higher
(specific) impact and soy has a seven-times higher (specific) impact compared with wheat, barley,
or rape (Table 4).

203
Sustainability 2018, 10, 3184

Table 4. The relative importance of crops in one tonne of feed at the present CO2 in terms of monetized
environmental impact. Due to the negative environmental impact that amino acids and some crops
have for various impact categories, the sum of the crop impact percentages surpasses 100%.

Importance of Crop Ingredients in Terms of Monetized Impact Wheat Barley Soy Rape Sunflower
Content, kg per tonne of feed (see Table 2) 480 250 92 68 42
Monetary weight of environmental impact, % 25 18 35 5 23
Monetized environmental impact relative to kg content, % 5.2 7.2 38.3 6.9 54.2
Factor of the above 1 1 7 1 11

In the context of a worldwide growing population with growing food and energy needs
(e.g., reference [49]), alternative strategies to minimize the amount of land that is used for food,
feed, or bioenergy are urgent. The main ingredients in compound pig feed could just as well be
consumed directly by humans. A pig consumes 2.5 times its weight gain in terms of pig feed before
only part of the pig ends up as food for humans (bones, head, and entrails are wasted). In a world with
a growing population and with about 800 million people starving, a more plant-based diet would make
sense, in terms of increasing food production, increasing the availability of bioenergy, and reducing
the environmental impact of global agriculture.
According to Table 4, future pig feed recipes ought to consider a reduced use of sunflower and
soy as protein crops. Whether rape or non-crop ingredients (e.g., industrial amino acids, insect-based
protein) would be a better environmental choice could be the object of future investigations. However,
since the value of protein in animal feed relies on the amino acid composition, it is important to
consider balancing the overall amino acid composition of the pig feed to suit the needs of pigs. In this
sense, industrial amino acids have a clear advantage, although economically it may not be the best
solution measured in the present commodity prices (as in this study). On the other hand, if and when
the cost of environmental impacts is included in the price of pig feed, it may likely be an advantage to
include more industrial amino acids in the feed.
An alternative or supplement to the above-mentioned solutions could be to include genetically
modified grain crops. These crops would need not only to contain more protein—which may in itself
be useless—but rather, they should contain more of the limiting amino acids for the better digestibility
of the protein in the feed.

3.5. Limits and Uncertainties

One limit of this study is that it focused only on the effect of elevated CO2 to represent the future
conditions under which pig feed will be produced. In fact, higher atmospheric CO2 is not the only
global change to determine the yield and the chemical composition of crops in the future. With elevated
CO2 follows elevated temperature and altered patterns of precipitation (10). Typically, crop yields
respond positively to both elevated CO2 and moderate (1–3 ◦ C) temperature increases, but negatively
to high (i.e., above 3 ◦ C) temperature increases [47,50]. Moreover, the response depends on the plant
species, water availability, humidity, wind, soil type, etc.
Furthermore, it has been highlighted that the current and anticipated elevated concentration
of ground-level ozone may likely decrease plant productivity [51]; and contrary to elevated CO2 ,
ozone increases grain protein concentration [51].
Thus, the results of this study are not to be seen as representative of the future state of global
climate and meteorological conditions (data for this is as yet unavailable), but rather as an illustration
of the cascading consequences that any change in crop yield and composition (which is in this case
triggered by an increase in atmospheric CO2 ) can have for pig feed formulation. As for any LCA,
the results of this study are closely linked to the quality of the inventory data and assumptions taken.
For example, no changes in amino acid composition were considered for barley and soy as a result of
elevated CO2 , because no data or reliable estimations could be found. Further, the overall changes
in yield and chemical composition considered (Table 1) are based on the best state-of-knowledge,

204
Sustainability 2018, 10, 3184

as available FACE experiments results are still scarce. Thus, this study would considerably benefit from
a greater availability of such data. Nevertheless, the study provides a solid framework for assessing
the consequences of a changed crop composition due to the effect that elevated atmospheric CO2
would have on pig feed, which has not, to authors’ knowledge, been available so far.
Another limit is that the changes in manure composition resulting from a change in feed
composition have not been taken into account. Feed containing less protein from cereals, which are
difficult to digest, and more easily digestible protein from e.g., soy or rapeseed meal, involves a better
digestion, and thus a reduction in excreted N. This could have consequences for the subsequent use
of the manure as a fertilizer, as it would involve a reduced potential for the emission of N flows
(e.g., ammonia, nitrous oxide, nitrate losses). Based on Table 2, these induced changes in manure
composition would likely have induced additional benefits for the future pig feed, which comprises
significantly more soymeal and less wheat.
One of the most important sources of uncertainty probably lies in the estimation of the
environmental consequences generated by land-use changes. As clearly emphasized in several
publications, e.g., references [52–54], the estimation of land-use changes, particularly ILUC,
involves multiple sources of uncertainty. In the explorative deterministic approach used in this
study, one main source of uncertainty lies in the choice of the market that would react to a changed
demand for the different crop ingredients presented in Table 2, i.e., the choice of the marginal crops
and their geographical location. Further, as expressed by e.g., reference [52] there is also uncertainty
related to the actual C stock in the biomes converted. On the other hand, the strength of the approach
used in this study lies in its transparency. In fact, the assumptions used in the deterministic model
can be easily changed to reflect different possible futures with regard to how the land market could
develop. However, such assessment is beyond the scope of this study. Nevertheless, it should be
highlighted that although the actual magnitude of environmental impacts related to land-use changes
is uncertain, the potentiality of adverse effects arising from it is hardly subject to dispute [25,53].
Finally, we draw the attention to the work by Dijkman et al. [55], where the environmental
impact of barley cultivation under current and future climatic conditions is analyzed using aLCA.
Dijkman et al. [55] found that a predicted decrease in barley yields under future climate conditions is
the main driver for increased impacts. An increased impact was not substantiated by the present study
based on cLCA and including all of the ingredients of compound pig feed.

4. Conclusions
The main findings and highlights of this study can be summarized as follows:

• A methodological framework was developed in order to assess the cascading environmental

consequences that a change in crop yield and chemical composition (triggered by an increase in
atmospheric CO2 ) can have for pig feed formulation, including land-use change consequences.
• The positive environmental effect of elevated CO2 on crop yield (carbohydrates) was counterbalanced
by a need for increased soy content in pig feed, and the land-use that consequences this generated.
Therefore, the net effects are close to zero.
• The four most important environmental impact categories in pig feed production under current
and future atmospheric CO2 , as determined by the stepwise normalization methodology,
were human toxicity in terms of non-carcinogenic toxicity and respiratory inorganics,
natural occupation, and global warming.
• The monetized environmental impact (shadow price) of compound pig feed produced today
(€236.05 per tonne) was found to be of the same order of magnitude as the direct price of compound
pig feed (€250.39 per tonne). Internalizing the cost of environmental impacts would nearly double
the price of pig feed if the Rio Declaration was to be honored.
• Since the protein crops (soy, rape, and sunflower) account for about 60% of the overall
environmental impact of pig feed, it is important to optimize their content in a future with

205
Sustainability 2018, 10, 3184

expected growing demands for food and bioenergy (and thus for land). In this context, it is
important to optimize the protein content in the feed based on the limiting amino acids in each
crop rather than on total protein.

Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/9/3184/

s1. References [56–64] are cited in the supplementary materials.
Author Contributions: Conceptualization: H.S.; Methodology, software, formal analyses and investigation: H.S.,
L.H., T.H.; Original Draft Preparation and visualization: H.S. and L.H.; Project Administration: H.S. and H.W.;
Funding Acquisition, H.W.
Funding: This research was funded by the Danish Food Research Programme 2009 for supporting this project
through grant number 3304-FVFP-09-B-004: “Development of genetically modified cereals adapted to the increased
CO2 levels of the future”.
Acknowledgments: The authors thank DLG for participating with Bestmix® analyses performed by
Torben Hinrichsen.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to
publish the results.

References
1. Högy, P.; Wieser, H.; Köhler, P.; Schwadorf, K.; Breuer, J.; Franzaring, J.; Muntefering, R.; Fangmeier, A.
Effects of elevated CO2 on grain yield and quality of wheat: Results from a 3-year free-air CO2 enrichment
experiment. Plant Biol. 2009, 11, 60–69. [CrossRef]
2. Smith, M.R.; Myers, S.S. Impact of anthropogenic CO2 emissions on global human nutrition. Nat. Clim. Chang.
2018, 8, 834–839. [CrossRef]
3. International Grain Council. Grain Marked Report. 2018; pp. 1–8. Available online: http://www.igc.int/
downloads/gmrsummary/gmrsumme.pdf (accessed on 14 August 2018).
4. Steinfeld, H.; Gerber, P.; Wasssenaar, T.; Castel, V.; Rosales, M.; de Haan, C. Livestock’s Long Shadow;
Environmental Issues and Options; FAO: Rome, Italy, 2006; pp. 1–390.
5. Nellemann, C.; MacDevette, M.; Manders, T.; Eickhout, B.; Svihus, B.; Prins, A.G.; Kaltennorn, B.P.
The Environmental Food Crisis–the Environment’s Role in Averting Future Food Crisis. A UNEP Rapid
Response Assessment. United Nations Environment Programme, GRID-Arendal. 2009. Available online:
http://www.grida.no/publications/rr/food-crisis/ (accessed on 14 August 2018).
6. Meul, M.; Ginneberge, C.; Van Middelaar, C.E.; de Boer, I.J.M.; Fremaut, D.; Haesaert, G. Carbon footprint of
five pig diets using three land use change accounting methods. Livest. Sci. 2012, 149, 215–223. [CrossRef]
7. Hamelin, L.; Naroznova, I.; Wenzel, H. Environmental consequences of different carbon alternatives for
increased manure-based biogas. Appl. Energy 2014, 114, 774–782. [CrossRef]
8. Searchinger, T.; Heimlich, R.; Houghton, R.A.; Dong, F.; Elobeid, A.; Fabiosa, J.; Tokgoz, S.; Hayes, D.;
Yu, T.-H. Use of U.S. Croplands for Biofuels Increases Greenhouse Gases through Emissions from Land Use
Change. Science 2008, 319, 1238–1240. [CrossRef] [PubMed]
9. Gibbs, H.K.; Johnston, M.; Foley, J.A.; Holloway, T.; Monfreda, C.; Ramankutty, N.; Zaks, D. Carbon payback
times for crop-based biofuel expansion in the tropics: The effects of changing yield and technology.
Environ. Res. Lett. 2008, 3, 1–10. [CrossRef]
10. IPCC, Climate Change 2014. Synthesis Report. 2015. Available online: https://www.ipcc.ch/pdf/
assessment-report/ar5/syr/SYR_AR5_FINAL_full_wcover.pdf (accessed on 14 August 2018).
11. Weidema, B.P.; Ekvall, T.; Heijungs, R. Guidelines for Applications of Deepened and Broadened LCA.
Deliverable D18 of Work Package 5 of the CALCAC Project. 2009; pp. 1–49. Available online:
https://www.leidenuniv.nl/cml/ssp/publications/calcas_report_d18.pdf (accessed on 14 August 2018).
12. Earles, J.M.; Halog, A. Consequential life cycle assessment: A review. Int. J. LCA 2011, 16, 445–453. [CrossRef]
13. Weidema, B.P. Using the budget constraint to monetarise impact assessment results. Ecol. Econ. 2008, 68,
1591–1598. [CrossRef]
14. Hamelin, L.; Jørgensen, U.; Petersen, B.M.; Olesen, J.E.; Wenzel, H. Modelling the carbon and nitrogen
balances of direct land use changes from energy crops in Denmark: A consequential life cycle inventory.
GCB Bioenergy 2012, 4, 889–907. [CrossRef]

206
Sustainability 2018, 10, 3184

15. Ecoinvent Centre. 2013. Available online: http://www.ecoinvent.org/database/ecoinvent-version-2/

(accessed on 14 August 2018).
16. Adifo. Bestmix Software. 2011. Available online: https://www.adifo.com/products/bestmix-feed-formulation
(accessed on 14 August 2018).
17. VSP, Videncenter for Svineproduktion, 2012. Fodermiddeldatabase (Feed Database). Available online:
https://www.lf.dk/aktuelt/nyheder/2015/april/ny-organisation-i-seges-videncenter-for-svineproduktion#
.W05DYtL7SUk (accessed on 14 August 2018).
18. Ainsworth, E.A.; Leakey, A.D.B.; Ort, D.R.; Long, S.P. FACE-ing the facts: Inconsistencies and
interdependence among field, chamber and modelling studies of elevated [CO2 ] impacts on crop yield and
food supply. New Phytol. 2008, 179, 5–9. [CrossRef] [PubMed]
19. Högy, P.; Fangmeier, A. Review: Effects of elevated atmospheric CO2 on grain quality of wheat. J. Cereal Sci.
2008, 48, 580–591. [CrossRef]
20. Mosnier, E.; van der Werf, H.M.G.; Boissy, J.; Dourmad, J.-Y. Evaluation of the environmental implications of
the incorporation of feed-use amino acids in the manufacturing of pig and broiler feeds using Life Cycle
Assessment. Animal 2011, 5, 1972–1983. [CrossRef] [PubMed]
21. Nielsen, P.H.; Wenzel, H. Environmental assessment of Ronozyme® P5000 CT phytase as an alternative to
inorganic phosphate supplementation to pig feed used in intensive pig production. Int. J. LCA 2007, 12,
514–520. [CrossRef]
22. Schmidt, J.H.; Weidema, B.P.; Brandão, M. A framework for modelling indirect land use changes in Life
Cycle Assessment. J. Clean. Prod. 2015, 99, 230–238. [CrossRef]
23. Tonini, D.; Hamelin, L.; Astrup, T.F. Environmental implications of the use of agro-industrial residues for
biorefineries: Application of a deterministic model for indirect land-use changes. GCB Bioenergy 2016, 8,
690–706. [CrossRef]
24. JRC. World Atlas of Desertification. 2018. Available online: https://wad.jrc.ec.europa.eu/ (accessed on
14 August 2018).
25. Marelli, L.; Mulligan, D.; Edwards, R.; Critical Issues in Estimating ILUC Emissions. Critical Issues
in Estimating ILUC Emissions. JRC Scientific and Technical Reports. Outcomes of an
Expert Consultation 9–10 November 2010, Ispra, Italy. 2011; pp. 1–64, EUR 24816EN-2011.
Available online: http://publications.jrc.ec.europa.eu/repository/bitstream/111111111/22908/2/reqno_
jrc64429_cirtical%20issues%20in%20estimating%20iluc%20emissions%20print%20version.pdf (accessed on
14 August 2018).
26. Verchot, L.V.; Davidson, E.A.; Cattânio, J.H.; Ackerman, I.L.; Erickson, H.E.; Keller, M. Land use change and
biogeochemical controls of nitrogen oxide emissions from soils in eastern Amazonia. Glob. Biogeochem. Cycles
1999, 13, 31–46. [CrossRef]
27. Wolosin, M.; Harris, N. Ending Tropical Deforestation: A Stock-Take of Progress and Challenges. Tropical
Forests and Climate Change: The Latest Science. 2018. World Resources Institute, Working Paper.
Available online: https://wriorg.s3.amazonaws.com/s3fs-public/ending-tropical-deforestation-tropical-
forests-climate-change.pdf (accessed on 14 August 2018).
28. De Lima, R.F.; Dallimer, M.; Atkinson, P.W.; Barlow, J. Biodiversity and land-use change: Understanding the
complex responses of an endemic-rich bird assemblage. Divers. Distrib. 2013, 19, 411–422. [CrossRef]
29. Nielsen, O.-K.; Mikkelsen, M.H.; Hoffmann, L.; Gyldenkærne, S.; Winther, M.; Nielsen, M.; Fauser, P.;
Thomsen, M.; Plejdrup, M.S.; Albrektsen, R.; et al. Denmark’s National Inventory Report 2011-Emission
Inventories 1990–2009-Submitted under the United Nations Framework Convention on Climate Change and the Kyoto
Protocol; NERI Technical Report 827; The National Environmental Research Institute, Aarhus University:
Aarhus, Denmark, 2011; pp. 1–1199. Available online: http://www2.dmu.dk/pub/fr827.pdf (accessed on
14 August 2018).
30. Schmidt, J.H. Life Cycle Assessment of Rapeseed Oil and Palm Oil. Ph.D. Thesis, Department of Development
and Planning, Aalborg University, Aalborg, Denmark, 15 June 2007.
31. Dalgaard, R.; Schmidt, J.; Halberg, N.; Christensen, P.; Thrane, M.; Pengue, W.A. LCA of soybean meal.
Int. J. LCA 2008, 13, 240–254. [CrossRef]

207
Sustainability 2018, 10, 3184

32. Edwards, R.; Mulligan, D.; Marelli, L. Indirect Land Use Change from Increased Biofuels Demand. Comparison
of Models and Results for Marginal Biofuels Production from Different Feedstocks. (No. EUR 24485). European
Commission Joint Research Centre. 2010. Available online: https://www.energy.eu/publications/Indirect-
Land-Use-Change-from-increased-Biofuels-Demand.pdf (accessed on 14 August 2018).
33. Hertel, T.W.; Golub, A.A.; Jones, A.D.; O’Hare, M.; Plevin, R.J.; Kammen, D.M. Effects of US Maize Ethanol
on Global Land Use and Greenhouse Gas Emissions: Estimating Market-mediated Responses. Bioscience
2010, 60, 223–231. [CrossRef]
34. Laborde, D. Assessing the Land Use Change Consequences of European Biofuel Policies. ATLASS Consortium,
2011. Available online: http://trade.ec.europa.eu/doclib/docs/2011/october/tradoc_148289.pdf (accessed on
14 August 2018).
35. Tonini, D.; Hamelin, L.; Wenzel, H.; Astrup, T. Bioenergy Production from Perennial Energy Crops:
A Consequential LCA of 12 Bioenergy Scenarios including Land Use Changes. Environ. Sci. Technol.
2012, 46, 13521–13530. [CrossRef] [PubMed]
36. Ekvall, T.; Weidema, B. System Boundaries and Input Data in Consequential Life Cycle Inventory Analysis.
Int. J. LCA 2004, 9, 161–171. [CrossRef]
37. Weidema, B.P.; Bauer, C.; Hischier, R.; Mutel, C.; Nemecek, T.; Reinhard, J.; Vadenbo, C.O.; Wernet, G.
The Ecoinvent Database: Overview and Methodology, Data Quality Guideline for the Ecoinvent Database
Version 3. 2017. Available online: https://lca-net.com/publications/show/overview-methodology-data-
quality-guideline-ecoinvent-database-version-3/ (accessed on 14 August 2018).
38. FAOSTAT. 2011. Available online: http://www.fao.org/faostat/en/#data (accessed on 14 August 2018).
39. De Vries, J.W.; Vinken, T.M.W.J.; Hamelin, L.; De Boer, I.M.J. Comparing environmental consequences
of anaerobic mono- and co-digestion alternatives for pig manure to produce bio-energy—A life cycle
perspective. Bioresour. Technol. 2012, 125, 239–248. [CrossRef] [PubMed]
40. Hamelin, L. Carbon Management and Environmental Consequences of Agricultural Biomass in a
Danish Renewable Energy Strategy. Ph.D. Thesis, University of Southern Denmark, Odense, Denmark,
February 2013.
41. Edwards, R.; Padella, M.; Vorkapic, V.; Marelli, L. Historical Deforestation Due to Expansion of Crop Demand:
Implications for Biofuels. 2014. Available online: http://publications.jrc.ec.europa.eu/repository/handle/
JRC83819 (accessed on 14 August 2018).
42. Erbs, M.; Manderscheit, R.; Jansen, G.; Seddig, S.; Pacholski, A.; Weigel, H.-J. Effects of free-air CO2
enrichment and nitrogen supply on grain quality parameters and elemental composition of wheat and barley
grown in a crop rotation. Agric. Ecosyst. Environ. 2010, 136, 59–68. [CrossRef]
43. Högy, P.; Franzaring, J.; Schwadorf, K.; Breuer, J.; Schütze, W.; Fangmeier, A. Effects of free-air CO2
enrichment on energy traits and seed quality of oilseed rape. Agric. Ecosyst. Environ. 2010, 139, 239–344.
[CrossRef]
44. Taub, D.R.; Miller, B.; Allen, H. Effects of elevated CO2 on the protein concentration of food crops:
A meta-analysis. Glob. Chang. Biol. 2008, 14, 65–575. [CrossRef]
45. Fangmeier, A.; Chrost, B.; Högy, P.; Krupinska, K. CO2 enrichment enhances flag leaf senescence in barley
due to greater grain nitrogen sink capacity. Environ. Exp. Bot. 2000, 44, 151–164. [CrossRef]
46. Morgan, P.B.; Bollero, G.A.; Nelson, R.L.; Dohleman, F.G.; Long, S.P. Smaller than predicted increase in
aboveground net primary production and yield of field-grown soybean under fully open-air [CO2 ] elevation.
Glob. Chang. Biol. 2005, 11, 1856–1865. [CrossRef]
47. Clausen, S.K.; Frenck, G.; Linden, L.G.; Mikkelsen, T.N.; Lunde, C.; Jørgensen, R.B. Effects of single and
multifactor treatment with elevated temperature, CO2 and ozone on oilseed rape and barley. J. Agron.
Crop Sci. 2011, 197, 442–453. [CrossRef]
48. Rio Declaration. 1992. Rio Declaration on Environment and Development. Principle 16.
Available online: https://www.jus.uio.no/lm/environmental.development.rio.declaration.1992/16.html
(accessed on 14 August 2018).
49. Nonhebel, S. Global food supply and the impacts of increased biofuels. Energy 2012, 37, 115–121. [CrossRef]
50. Qaderi, M.M.; Reid, D.M. Crop Responses to Elevate Carbon Dioxide and Temperature; Singh, S.N.,
Ed.; Chapter 1 in: Climatic Change and Crops, Environmental Science and Engineering; Springer:
Berlin/Heidelberg, Germany, 2009; pp. 1–17.

208
Sustainability 2018, 10, 3184

51. Booker, F.; Muntifering, R.; McGrath, M.; Burkey, K.; Decoteau, D.; Fiscus, E.; Manning, W.; Krupa, S.;
Chappelka, A.; Grantz, D. The ozone component of global change: Potential effects on agricultural and
horticultural plant yield, product quality and interactions with invasive species. J. Integr. Plant Biol. 2009, 51,
337–351. [CrossRef] [PubMed]
52. Plevin, R.J.; O’Hara, M.; Jones, A.D.; Torn, M.S.; Gibbs, H.K. Greenhouse Gas Emissions from Biofuels’
Indirect Land Use Change Are Uncertain but May Be Much Greater than Previously Estimated.
Environ. Sci. Technol. 2010, 44, 8015–8021. [CrossRef] [PubMed]
53. Khanna, M.; Crago, C.L. Measuring Indirect Land Use Change with Biofuels: Implications for Policy.
Annu. Rev. Resour. Econ. 2012, 4, 161–184. [CrossRef]
54. Sanchez, S.T.; Woods, J.; Akhurst, M.; Brander, M.; O’Hara, M.; Dawson, T.P.; Edwards, R.; Liska, A.J.;
Malpas, R. Accounting for indirect land-use change in the life cycle assessment of biofuel supply chains. J. R.
Soc. Interface 2012, 9, 1105–1119. [CrossRef] [PubMed]
55. Dijkman, T.J.; Birkved, M.; Saxe, H.; Wenzel, H. Environmental impacts of barley cultivation under current
and future climatic conditions. J. Clean. Prod. 2017, 140, 644–653. [CrossRef]
56. Kløverpris, J. Consequential Life Cycle Inventory Modelling of Land Use Induced by Crop Consumption.
Ph.D. Thesis, DTU Management Engineering, Lyngby, Denmark, November 2008. Updated Version 2010.
Available online: http://orbit.dtu.dk/en/publications/consequential-life-cycle-inventory-modelling-of-
land-use-induced-by-crop-consumption%286457fc93-c53a-4beb-83ff-015c8047b682%29.html (accessed on
14 August 2018).
57. Jungbluth, N.; Dinkel, F.; Doka, G.; Chudacoff, M.; Dauriat, A.; Gnansounou, E.; Sutter, J.; Spielmann, M.;
Kljun, N.; Keller, M. Life Cycle Inventory of Bioenergy. Data v2.0. Ecoinvent Report no. 17. Swiss Centre for
Life Cycle Inventories. A Joint Initiative of the ETH Domain and Swiss Federal Offices, Ulster, Switzerland.
Available online: https://www.researchgate.net/profile/Niels_Jungbluth/publication/230725648_Life_
Cycle_Inventories_of_Bioenergy_ecoinvent_report_No_17/links/0c96051b76e2fb8dce000000/Life-Cycle-
Inventories-of-Bioenergy-ecoinvent-report-No-17.pdf (accessed on 14 August 2018).
58. Schmidt, J.H.; Christensen, P.; Christensen, T.S. Assessing the land use implications of biodiesel use from an
LCA perspective. J. Land Use Sci. 2009, 4, 35–52. [CrossRef]
59. Nemecek, T.; Kägi, T. Life Cycle Inventory of Agricultural Production Systems. Data ver. 2.0. Ecoinvent
Report no. 15. Agroscope Reckenholz-Tänikon Research Station ART, Zürich and Dübendorf, Switzerland.
Available online: https://db.ecoinvent.org/reports/15_Agriculture.pdf (accessed on 14 August 2018).
60. Miyagi, K.-M.; Kinugasa, T.; Hikosaka, K.; Hirose, T. Elevated CO2 concentration, nitrogen use, and seed
production in annual plants. Glob. Chang. Biol. 2007, 13, 2161–2170. [CrossRef]
61. Buckley, T.N. The role of stomatal acclimation in modelling tree adaptation to high CO2 . J. Exp. Bot. 2008, 59,
1951–1961. [CrossRef] [PubMed]
62. Attavanich, W.; McCarl, B.A. The effect of climate change, CO2 fertilization, and crop production technology
on crop yields and its economic implications on market outcomes and welfare distribution. In Proceedings
of the Agricultural & Applied Economics Association’s 2001 AAEA & NAREA Joint Annual Meeting,
Pittsburgh, PA, USA, 24–26 July 2011.
63. Sprague, G.F.; Duncan, W.G.; Kommedahl, T.; BeMiller, J.N. Corn. In AccessScience, ® McGraw-Hill
Companies. 2008. Available online: https://www.accessscience.com/content/corn/162600 (accessed on
14 August 2018).
64. Cederberg, C.; Flysjö, A. Environmental Assessment of Future Pig Farming Systems–Quantification of Three
Scenarios from the FOOD 21 Synthesis Work. SIK Rapport nr. 723. SIK, Sweden. 2004. Available online:
http://www.vaxteko.nu/html/sll/institutet_livsm_bioteknik/sik-rapport/SIK723/SIK723.PDF (accessed on
14 August 2018).

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

209
 sustainability

Article
Cattle Diets Strongly Affect Nitrous Oxide in
the Rumen
Katrin Gerlach 1, * , Alexander J. Schmithausen 2 , Ansgar C. H. Sommer 1 , Manfred Trimborn 2 ,
Wolfgang Büscher 2 and Karl-Heinz Südekum 1
1 Institute of Animal Science, University of Bonn, 53115 Bonn, Germany;
[email protected] (A.C.H.S.); [email protected] (K.-H.S.)
2 Institute of Agricultural Engineering, University of Bonn, 53115 Bonn, Germany;
[email protected] (A.J.S.); [email protected] (M.T.); [email protected] (W.B.)
* Correspondence: [email protected]; Tel.: +49-228-732281

Received: 5 October 2018; Accepted: 12 October 2018; Published: 14 October 2018

Abstract: This study aimed at assigning climate-relevant gaseous emissions from ruminants to
animal- or feed-related origin. Three adult rumen-cannulated German Holstein steers and three
forage types (corn silage (CS), alfalfa silage (AS) and grass hay (GH)) were used in a 3 × 3 Latin
square design. Each period consisted of 12 days (d), during which animals received 10 kg dry
matter/day of one forage as sole feed. Gaseous samples from forages and the steers´ rumen were
taken and analyzed for CO2 , CH4 , and N2 O using gas chromatography. There were large differences
in the amounts of CO2 and N2 O emitting from the forage types. Most N2 O came from AS and only
small amounts from GH and CS. Results indicate that fermented forages rich in nitrogen can release
climate-relevant N2 O. The highest CO2 amounts were measured in CS. Methane was not detected in
any forage sample. Animals consuming CS showed slightly lower CH4 concentrations in the rumen
gas sample than animals fed AS or GH. Big differences were found for ruminal N2 O with the highest
concentration after AS ingestion such that the N2 O measured in the rumen seems to originate from
the used feedstuff.

Keywords: cow; greenhouse gas; methane; rumen; silage

1. Introduction
Animal production significantly contributes to climate-relevant greenhouse gas (GHG) emissions
but also offers considerable reduction potential such that different mitigation strategies like the use
of feed additives and application of feeding strategies as well as different manure, reproduction,
and animal management strategies are discussed [1,2]. Ruminants are mainly responsible for the trace
gases methane (CH4 ) and nitrous oxide (N2 O) with the latter having a much higher carbon dioxide
(CO2 ) equivalence factor (298) than CH4 (25) [3]. Methane is a product of the anaerobic fermentation of
carbohydrates in the rumen, which is a pathway for the disposal of hydrogen formed during microbial
metabolism [4]. Cattle lose 2–10% of their ingested gross energy as eructated CH4 [5], and the total
amount is influenced by dry matter (DM) intake (DMI) and ration composition [6–8]. The volatile
N2 O (Henry´s law constant, k◦ H 0.025 mol/kg × bar) is mainly produced by the microbially facilitated
denitrification in manure and to a smaller extent by nitrification in soils [9]. The contribution of GHG
emissions from enteric fermentation and manure management occurs in a ratio of about 9:1 [10] such
that the potential for decreasing GHG emissions is mainly seen in manipulating enteric fermentation,
e.g., by adjusting composition of rations. In this regard, different studies have already been performed
using in vitro and in vivo measurements (e.g., recent work by Lee et al. [11] and Macome et al. [12]) as
well as rumen-cannulated cows, among others resulting in different regression equations for predicting
CH4 emissions based on intake and diet characteristics [13]. When applying different regression

Sustainability 2018, 10, 3679; doi:10.3390/su10103679 210 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3679

equations to five typical Central European dairy cow rations it was shown that the best differentiation
between diets was achieved with equations containing forage proportion and DMI as factors [13].
For measurement of GHG emissions on animal level the use of respiration chambers is a proven
technology [5,14]. Other techniques comprise a mobile open-circuit hood system to measure the gas
exchange in small ruminants [15] and a ventilated hood system for measuring GHG from cattle [16].
Most studies focused on emissions of CH4 and CO2 , whereas approaches investigating the effect of
ration composition on enteric emissions of N2 O are rare [17,18]. Rotz and Thoma [19] reviewed that
N2 O emissions are in the range of 0.3–0.5 g/cow per day (d), with higher values occurring possibly
under certain dietary conditions. Authors state that mechanisms and amount produced are generally
not well understood but that high dietary nitrate (NO3 − ) levels might induce increased N2 O emissions.
Though, they also agree that more research is needed to better quantify that source of emission as
formation in the rumen is questionable [20].
However, beside the ruminant itself, the forage used as feedstuff can also act as a source of
emissions: for non-fermented forages Emery and Mosier [21] measured emissions of CO2 , CH4 ,
and N2 O from switchgrass and corn stover under varying storage conditions. Both CH4 and N2 O
were detected and concentrations were influenced by forage DM concentration. However, when
calculating the net global warming potential for the different treatments (0–2.4 g CO2 equivalents/kg
DM) authors suggested that direct emission of CH4 and N2 O from aerobically stored (non-fermented)
feedstuffs have a minor effect on net global warming potential of cellulosic biofuels. Fermented forages
as an origin of gaseous emissions measured in the environment of ruminants have rarely been studied.
In early studies of Wang and Burris [22] N2 O was detected in whole-crop corn silages where the gas
composition was analyzed eight times within 66 h after sealing the silo. A constant increase in N2 O
concentration from 1.50% (v/v) to 4.55% after 54 h was measured which declined afterwards to 1%.
The origin of the N2 O was seen in the reduction of NO3 − [22]. The reduction of NO3 − starts a few
hours after ensiling with an enrichment of the intermediate products NO und NO2 − which normally
disappear after one or two weeks of ensiling [23]. Further reduction by Enterobacteriaceae results in
N2 O and ammonia (NH3 ) [24]. Also recent work using Fourier transform infrared (FTIR) spectroscopy
verified the presence of N2 O in gases formed in the early phase of ensilage of whole-crop corn [25].
Franco [26] showed that particularly forages naturally rich in nitrogen (N), especially in the form of
nitrate, had significant N2 O production during silage fermentation. Up to now, only little attention has
been given to N2 O possibly emitting during the feed-out phase of silages.
Gaseous emissions occurring in the environment of ruminants are often difficult to assign to a
specific source (e.g., feed, rumen, manure), especially when measurements are conducted on barn
level, in respiration or environmental chambers. This impedes the explanation of their formation and
strategies for mitigation.
Therefore, the objective of the present study was to determine gaseous emissions from ruminants
offered different forage types (corn silage (CS), alfalfa silage (AS) and grass hay (GH)) with contrasting
chemical composition and to assign the emissions to animal or feed-related sources, with special
emphasis on nitrous oxide. To the best of our knowledge, this is the first study determining the
concentration of CO2 , CH4 , and N2 O in the ruminal gas phase of steers after ingestion of three different
forage types.

2. Materials and Methods

2.1. Animals, Diets, and Experimental Design

This study was conducted at the Educational and Research Center Frankenforst of the Faculty
of Agriculture, University of Bonn (Königswinter, Germany). All experimental procedures were
conducted in accordance with the German guidelines for animal welfare and were approved (file
number 84-02.04.2017.A247) by the Animal Care Committee of the state of North Rhine-Westphalia.
Three animals and three forage types differing in chemical composition (CS, AS, GH) were used.

211
Sustainability 2018, 10, 3679

Three adult rumen-cannulated German Holstein steers (born and raised on the Center, 4 years old,
rumen-cannulated since 2 years, about 1300 kg body weight) were housed separately in single pens
(4.4 × 4.6 m) allowing visual contact. Ambient conditions within the barn were consistent throughout
the experimental period with a temperature of 18.4 ± 2.1 ◦ C and relative air humidity of 74.7 ± 8.3%.
Water was continuously available allowing ad libitum intake. The whole trial consisted of 42 d (4 June
to 15 July 2016) and was divided into three periods following a 3 × 3 Latin square design. Each period
started with a 2-d adaptation phase during which animals were offered a ration consisting of 50% of
the previous forage and 50% of the new forage. Twelve days of experimental feeding followed during
which animals received one of the three forages as sole feed. During this time, each steer was offered
10 kg DM/d of the respective forage. Measurement of gaseous emissions was carried out during
the last 3 d of each period. Table 1 shows the chemical composition of the forages which had been
produced at the Educational and Research Center Frankenforst. The AS was produced from a fourth
cut of alfalfa (harvest date 9 September 2015) and ensiled in round bales. For CS, the whole-crop corn
(harvest date 20 September 2015) was chopped (6 mm theoretical chop length) and ensiled in a bunker
silo. The GH was made from the second cut (harvest date 28 June 2015), and the field-dried hay was
packed in round bales. To ensure constant forage qualities during each period, silages were stored
anaerobically in 120-L plastic barrels. Therefore, the CS was taken from a fresh silage face and the
AS was obtained from a round bale opened just before. Silages were filled into the barrels in several
layers, each layer was compacted separately such that a high density was reached, and were then
stored anaerobically. Forages were offered to the steers once daily at 08.00 a.m. Before feeding in
the morning, remaining feed was removed and weighed to determine DMI. During the last 3 d of
each period (sampling period), the DM consumed within 180 min after offering feed in the morning
was also measured. Every day (d 10–12), a representative sample (500 g) of each forage was taken
and composited to one sample for each period. After sampling, forages were immediately frozen
until analysis.

Table 1. Chemical composition of forages used for the gaseous measurements and as feedstuffs for the
steers (expressed as g/kg dry matter (DM) unless stated; (n = 3)).

Corn Silage (CS) Alfalfa Silage (AS) Grass Hay (GH)

DM [g/kg] 366 415 881
Ash 34.9 124 70.5
Crude protein 70.7 246 79.2
Ether extract 35.9 30.2 20.2
aNDFom 1 314 396 599
ADFom 2 175 300 340
Acid detergent lignin 17.4 98.3 36.8
Starch 438 n.a. n.a.
In vitro gas production [mL/200 mg DM] 64.1 39.8 50.5
Metabolizable energy [MJ/kg DM] 11.7 8.78 9.40
pH 3.9 5.77 n.a.
Lactic acid 40.7 8.2 n.a.
Acetic acid 9.9 6.3 n.a.
Butyric acid n.d. 3 n.d. n.a.
Methanol 0.3 1.5 n.a.
Ethanol 1.7 1.6 n.a.
Water-soluble carbohydrates 13.4 49.8 n.a.
NH3 -N [g/kg total N] 109 96.7 n.a.
Ethyl acetate [mg/kg DM] 54.4 19.3 n.a.
Ethyl lactate [mg/kg DM] 105 n.d. n.a.
1 aNDFom: neutral detergent fiber assayed with heat-stable amalyse and expressed exclusive residual ash. 2

ADFom: acid detergent fiber expressed exclusive residual ash. n.d.: not detected. n.a.: not analyzed.

212
Sustainability 2018, 10, 3679

2.2. Sampling and Measurements of Gaseous Emissions

During the last 3 d of each period, sampling for measurements of gaseous emissions from forages
and the rumen was conducted. Concurrently, forage samples for laboratory analysis and incubation
experiments for gas measurement were taken. The emission measurements aimed at the acquisition of
the gases CO2 , CH4 , and N2 O from the forages and the rumen gas of the steers. Sampling of emissions
from the forages was conducted simultaneously to the feeding using closed containers with a volume
of 10 L. The containers were made of polyethylene (PE) and were equipped with a rubber septum
for gas sampling via twin needle. For each container, average temperature and relative humidity
were logged continuously using data loggers (Tinytag Plus 2—TGP-4500, Gemini Data Loggers Ltd.,
Chichester, West Sussex, UK). For sample collection a defined amount of each forage (1 kg each of
CS and AS, and 0.5 kg GH) was put in the container and sealed gas tight. Within the next 40 min
five gaseous samples were taken using evacuated headspace vials directly after closure (0 min) and
10, 20, 30, and 40 min after closure (Figure 1a). Then the containers were opened for 140 min to
enable unrestricted, natural air exchange before a second sealing and gas sampling period started.
The headspace vials had a vacuum range below 5 mbar. The vacuum was produced by pricking a
twin needle through the container septum as described by Schmithausen et al. [27]. This procedure
(sampling of emissions from the forages) was conducted on 3 consecutive d.

(a) (b)
Figure 1. Sampling (a) of gaseous emissions from the forages stored in a closed container via headspace
vials and (b) from the gaseous phase of the rumen with a syringe through the closed lid of the
rumen-cannula (left) and filling into a headspace vial (right).

Samples from the gaseous phase of the steers´ rumen were taken 180 min after offering feed in the
morning. In 10-min intervals (0, 10, 20, and 30 min), one sample was obtained with a syringe (50 mL)
through the closed lid of the rumen-cannula and filled into two evacuated headspace vials (20 mL each;
Figure 1b). Subsequently, samples were analyzed for CO2 , CH4 , and N2 O using a gas chromatograph
(GC) (8610 C, SRI Instruments, Torrance, CA, USA). The N2 O and CO2 were determined with an
electron capture detector (ECD) and CH4 was measured with a flame ionization detector (FID) [28,29].
The detection limit of the used analytical technique for CO2 , CH4 , and N2 O is described in detail by
Schmithausen et al. [30]. The emission rates of the respective gas from the incubation experiments

213
Sustainability 2018, 10, 3679

were calculated via linear regression of the gas concentration over time, more specifically, the slope
of the regression line. The detection limits of the GC result in minimally measurable increases in the
concentration (slope) of the investigated gases in the incubation experiment. In the case of CH4 , for
example, this minimum slope was 0.5 ppm CH4 , which corresponds to 3.3 μg CH4 /(kg of feed × h).
Comparable measurements by using headspace vials and defined criteria of evaluation are described
by Schmithausen et al. [27]. As a result of the ruminal gas analysis, the concentrations of CH4 in rumen
gas phase and the ratio of N2 O to the sum of CO2 and CH4 are shown. The amounts of N2 O formed in
the rumen or the emission rates of N2 O from the rumen could not be calculated, as the total volume of
air in the rumen and the total rates of formation of CO2 and CH4 in the rumen could not be determined
in this experiment. The CO2 , N2 O, and CH4 values are expressed as concentration in the rumen gas
phase as well as ratio of CH4 to CO2 as an indicator of the efficiency of microbial fermentation [31].

2.3. Laboratory Analyses of the Forages

In each of the three periods, silages and hay were sampled for chemical analyses. Forages were
kept at −20 ◦ C and were then freeze-dried (Freeze-Dryer P18K-E, Piatkowski Forschungsgeräte,
München, Germany) in triplicate. Afterwards, a duplicate subsample was oven-dried overnight
at 105 ◦ C for determination of the DM concentration. A correction of DM (DMcor) for the
losses of volatiles during drying was done in alfalfa and corn silages with the following equations
(concentrations are given as g/kg):

Alfalfa silage [32]:

DMcor = DM + (1.05 − 0.059 × pH) × total volatile fatty acids (VFA, C2 − C6 ) +

(1)
0.08 × lactic acid + 0.77 × 1,2-propanediol + 0.87 × 2,3-butanediol + 1.00 × total of other alcohols.

Corn silage [33]:

DMcor = DM + 0.95 × VFA (C2 − C6 ) + 0.08 × lactic acid +
(2)
0.77 × 1,2-propanediol + 1.00 × other alcohols.

After freeze-drying, samples were ground using 3-mm and afterwards 1-mm sieves. Samples
were chemically analyzed according to VDLUFA [34] and following method numbers: Analysis of
ash and ether extract (EE) was done by using methods 8.1 and 5.1. Crude protein (CP) was analyzed
by Dumas combustion (4.1.2, FP328, Leco 8.1, Leco Instrumente, Mönchengladbach, Germany).
The concentrations of neutral detergent fiber assayed with heat-stable amylase and expressed exclusive
residual ash (aNDFom; 6.5.1), acid detergent fiber expressed exclusive residual ash (ADFom; 6.5.2),
and acid detergent lignin (ADL; 6.5.3) were determined with an Ankom2000 Fiber Analyzer (Ankom
Technology, Macedon, NY, USA). Following point 8.8 of method 6.5.2 the analysis of ADFom was
conducted sequentially for AS to avoid precipitation of pectins. In CS, the concentration of starch was
determined after enzymatically hydrolyzing starch to glucose [35]. The 24 h in vitro gas production (GP
[mL/200 mg DM]) of forage samples was measured with the Hohenheim gas test (method 25.1, [34])
and afterwards, the concentration of metabolizable energy (ME) was estimated as follows:

Corn silage [36]:

ME = 0.136 × GP + 0.0057 × CP + 0.000286 × EE2 + 2.20. (3)

Alfalfa silage [37]:

ME [MJ/kg organic matter] = 11.09 − 0.01040 × ADFom + 0.00497 × CP + 0.00750 × EE +

(4)
0.0351 × GP; ME [MJ/kg DM] = ME (MJ/kg organic matter) × [1000 − ash (g/kg DM)]/1000.

Grass hay [38]:

ME = 7.81 + 0.07559 × GP + 0.00384 × ash + 0.00565 × CP + 0.01898 × EE − 0.00831 × ADFom. (5)

214
Sustainability 2018, 10, 3679

Both silage types were analyzed for fermentation products after cold-water extraction. These
analyses were conducted at the Central Analytical Laboratory of the Humboldt University, Berlin,
Germany and concentrations of lactic acid, volatile fatty acids (VFA), alcohols (methanol, ethanol,
propanol, 1,2-propanediol, 2,3-butanediol), acetone, ammonia, and water-soluble carbohydrates (WSC)
as well as the pH were determined. Frozen forage samples (50.0 g) were blended with a mixture of
200 mL distilled water and 1 mL toluene for preparation of cold-water extracts. After keeping them
overnight in a refrigerator extracts were filtered with a folded filter paper. The pH in the extract was
measured potentiometrically with a calibrated pH electrode. Analysis of lactic acid was done by high
performance liquid chromatography (HPLC) (RI-detector, Shimadzu Deutschland GmbH, Duisburg,
Germany) [39]. Gas chromatography with FID (GC-2010; Shimadzu Deutschland, Duisburg, Germany)
and a free fatty acid phase column (Permabond FFAP 0.25 Tm; Macherey-Nagel, Düren, Germany)
was used for determining the VFA and alcohols. Ammonia was measured colorimetrically using a
continuous flow analyzer (Skalar Analytical B.V., Breda, The Netherlands) and the concentration of
WSC was analyzed using the anthrone method [40].

2.4. Statistical Analyses

All statistical analyses were performed with SAS 9.4. The following mixed model was used for
the rumen samples:
yij = μ + Fi + Pj + (F × P)ij + Ak + eijk (6)

with y = observed response; μ = overall mean; Fi = fixed effect of forage type i = 1, 2, 3; Pj = fixed effect
of period j = 1, 2, 3; (B × P)ij = effect of interaction forage type I × period j; A = random effect of the
animal k = 1, 2, 3; and eijk = residual error.
For analysis of the gas samples from forages the following mixed model was used:

yij = μ + Fi + Pj + (F × P)ij + eij (7)

y = observed response; μ = overall mean; Fi = fixed effect of forage type i = 1, 2, 3; Pj = fixed effect of
period j = 1, 2, 3; (B × P)ij = effect of interaction forage type I × period j; and eij = residual error.
Covariance structures were tested with the types “unstructured“, “autoregressive“, and
“compound symmetry“. ”Akaike´s Information Criterion“ (AIC) was used to decide which model
showed the best fit and based on that, “autoregressive” was chosen for the analysis. Within the
period, d was taken as a repeated measurement. Least squares means were compared using the PDIFF
option in SAS. Significant treatment effects were detected by pairwise comparisons employing Tukey´s
test. In all statistical analyses, differences among means with p < 0.05 were accepted as representing
statistically significant differences.

3. Results

3.1. Gas Production from Forages

As intended, forages differed considerably in chemical composition (Table 1). The AS had high
concentrations of CP (246 g/kg DM), whereas GH and CS had only low to moderate concentrations.
The GH contained high concentrations of fiber fractions (e.g., aNDFom) and was low in EE. The CS
was high in starch (438 g/kg DM), in vitro gas production and metabolizable energy. Both silage types
were well fermented with moderate to low concentrations of acetic acid and without butyric acid.
The pH value in AS, however, was higher than recommended.

215
Sustainability 2018, 10, 3679

The emissions from forages as influenced by forage type, period, and their interaction are shown
in Table 2. There were large differences in the rates of CO2 and N2 O emitting from the forages
(p < 0.05). Most N2 O was released from AS (24.1 μg/(kg DM × h)) and only small amounts from GH
(0.233 μg/(kg DM × h)) and CS (0.109 μg/(kg DM × h)). The CO2 emissions were also influenced by
forage type and greatest CO2 amounts were measured in CS, followed by AS (p < 0.01). Both N2 O
and CO2 were influenced by forage type, but no influence (p > 0.05) was observed of period or the
interaction between period and forage type. After 180 min, most emissions from forages were strongly
reduced but 170 mg/(kg DM × h) of CO2 were still emitting from CS. Methane was not detected in
any forage sample, neither directly after silo opening nor after 180 min (detection limit for CH4 was
3.3 μg/(kg × h)).

Table 2. Effect of forage type (F) and period (P) on emission rates of CH2 and N2 O * of samples
obtained from corn silage (CS), alfalfa silage (AF) and grass hay (GH) directly after silo opening (8 a.m.)
and after 180 min of air exposure (11 a.m.).

Least Square Means Effect

CS AS GH SEM F P F·P
N2 O [μg/(kg dry 8 a.m. 0.109 b 24.1 a 0.233 b 3.81 0.02 n.s. n.s.
matter × h)] 11 a.m. 0.140 b 2.46 a 0.176 b 0.172 <0.01 0.01 <0.01
CO2 [mg/(kg dry 8 a.m. 391 a 141 b 8.13 c 32.0 <0.01 n.s. n.s.
matter × h)] 11 a.m. 170 a 19.0 b 9.38 b 14.4 <0.01 n.s. n.s.
* Methane was not detected in any forage sample. SEM: standard error of the mean. n.s.: not significant (p < 0.05).
a–c Values within a row with different letters are significantly (p < 0.05) different.

3.2. Gas Composition in the Rumen

The effect of forage type and period on DMI and composition of gaseous samples obtained
from the rumen of steers is shown in Table 3. During 180 min, animals consumed 3.3 to 6.6 kg
DM which was influenced by forage type. 180 min after initiation of feed ingestion, gas samples
were taken from the rumen. There was a significant effect of forage type on all measured variables
(p < 0.01). Big differences were found for N2 O with higher concentrations for AS than for CS and
GH (p < 0.01). The N2 O concentration in the rumen atmosphere relative to the sum of CH4 and
CO2 (%) for the different forage types obtained from the single measurements is shown in Figure 2.
Elevated concentrations were only detected after ingestion of AS. Animals fed CS showed slightly
lower CH4 concentrations in the rumen gas sample than when fed AS or GH. The CH4 to CO2 ratio
was highest for AS (p < 0.01) and there was no difference between CS and GH (p > 0.05). This ratio can
be seen as an indicator of the efficiency of microbial fermentation as it directly describes the share of
emitted C that has not been metabolized to CO2 [31].
The CO2 concentration was highest after ingestion of GH (p < 0.01) and did not differ between
CS and AS (p > 0.05). The remaining gas (difference to 100%) that cannot be explained by CH4 , CO2 ,
and N2 O is presumably atmospheric air that may have entered the rumen or the gaseous sample via
three possible ways: with the forage into the rumen during ingestion, via small leakages of the rumen
cannula into the rumen or during sampling (into evacuated headspace vials). Concentrations of both
O2 and N2 typically increase during feeding [41]. As oxygen entering during ingestion or via the
cannula is depleted rapidly in the rumen atmosphere, mainly N2 remains from the atmospheric air
which could not be analyzed with the methodology applied in this study.

216
Sustainability 2018, 10, 3679

Table 3. Effect of forage type (F) and period (P) on dry matter intake (DMI) over 180 min and
composition of gaseous samples obtained from the rumen of steers 180 min after initiation of feed intake.

Least Square Means Effect

Corn Silage Alfalfa Silage Grass Hay
SEM F P F·P
(CS) (AS) (GH)
DMI [kg/180 min] b b 6.64 a 0.473 <0.01 0.02 <0.01
4.60 3.22
N2 O [ppm] 0.246 b 0.857 a 0.171 b 0.068 <0.01 n.s. 0.02
CH4 [%] 16.9 b 20.6 a 20.3 a 0.890 0.01 <0.01 0.03
CO2 [%] 46.1 b 41.1 b 54.8 a 2.21 <0.01 n.s. 0.03
CH4 :CO2 0.358 b 0.501 a 0.372 b 0.010 <0.01 0.02 <0.01
a–c Values within a row with different letters are significantly (p < 0.05) different. SEM: standard error of the mean.
n.s.: not sigificant (p > 0.05).

Figure 2. The N2 O concentration (ppm) in the rumen gas relative to the CH4 +CO2 concentration (%)
for alfalfa silage, corn silage, and grass hay.

4. Discussion

4.1. Emissions from Forages

Directly after silo opening, N2 O emitted from AS but there were no N2 O emissions from CS
and GH. Formation of N2 O during ensiling has been described before and can be mainly ascribed
to anaerobic activity of Enterobacteriaceae species occurring during the initial period of ensiling [23].
Plant enzymes, on the other hand were not capable of producing N2 O and NOx during ensiling such
that microbial activity seems to be the main underlying process [26]. The conversion of NO3 − during
ensiling appears to be related to the duration the crop remains at a pH at which Enterobacteriaceae
may grow and utilize NO3 − (pH > 4.5–5.0) [24]. Due to a typically high buffering capacity (high
CP, high ash concentration) and a high DM concentration of the experimental AS only a moderate
drop in pH to 5.7 had been achieved. Consequently Enterobacteriaceae were not restricted by acidic
conditions during the whole storage period. Also the increased NH3 -N concentrations in AS may
reflect increased activity of Enterobacteriaceae [23]. In contrast to this, whole-crop corn typically has
a low buffering capacity and ferments rapidly. As a result, the CS had a low pH (3.9) which inhibits
Enterobacteriaceae. The N2 O emissions from CS and GH were very low and only slightly above detection
limit (0.1 μg/(kg × DM h)).

217
Sustainability 2018, 10, 3679

Aerobic activity of Enterobacteriaceae may also occur in silages [42], but is most probably restricted
to respiration. The decreased emission rates of N2 O after 180 min of air exposure indicate that N2 O
emitted that had already been formed during the anaerobic fermentation process. The major part
of the N2 O was released during 180 min such that an aerobic formation seems unlikely. It can be
concluded that N2 O emissions from forages are possible under certain circumstances. It seems to be
most pronounced from forages with high CP and NO3 − concentrations at harvest [26] and extended
and/or continuous activity of Enterobacteriaceae which can be caused by high silage pH [24]. It is
therefore important to optimize the ensiling conditions (rapid wilting and sealing, strong compaction,
use of additives in substrates that are classified as being difficult to ensile) to ensure a fast and sufficient
drop in pH. More research is needed to state more precisely the conditions of formation and release of
N2 O in silages. However, the total amounts of N2 O emitting from fermented forages are much lower
than typical emissions from manure during storage which are in the range of 1.0 to 3.0 kg/cow per
year (equaling 0.1 to 0.3 g/cow per h), mainly depending on the method of storage [19].
Besides N2 O, also CO2 emitted from forages with an effect of forage type. As expected, only
fermented forages released considerable amounts of CO2 , most likely produced at the beginning of the
ensiling process. The CS emitted more CO2 than AS. Caused by its plant structure and longer chop
length in comparison to CS, alfalfa is more difficult to compact and its tubular hollow stem may even
impede the removal of air during ensilage [43] or, vice versa, facilitate ingress of oxygen as soon as the
silo is opened. Therefore, CO2 might be lower in concentration and emit very quickly after silo opening
or during relocation to the barrels, explaining the lower emission rates in AS. Also aerobic spoilage
processes by yeasts and molds which typically take place after silo opening lead to the formation of
CO2 [44]. However, as CS still had a low pH and high concentrations of lactic acid (as an indicator of
good fermentation quality) and emission rates diminished during aerobic exposure, ongoing aerobic
deterioration processes can be excluded and the measured CO2 might result from gassing out of CO2
already being formed during ensiling. The forage gas samples were also analyzed for CH4 but changes
in concentration were below detection limit in all cases. Fermented forages seem to be an unlikely
source of CH4 emissions. To the best of our knowledge, possible CH4 emissions from silages have
also not been studied or discussed in literature. Emery and Mosier [21] measured GHG emissions
from unfermented feedstuffs and detected small amounts of CH4 ; however impact on the net global
warming potential was assessed to be small.

4.2. Concentration Ratios in the Rumen

With the method of taking samples through the closed lid of the rumen-cannula via a syringe
it was possible to obtain information on the composition of the gaseous phase in the rumen of
the steers, without any interference (e.g., atmospheric air, oral contact, manure). Highest ruminal
concentrations of N2 O were found for steers fed AS with values exceeding 2.5 ppm at some sampling
times (Figure 2) despite the fact that DMI was lowest for AS. In contrast, the N2 O concentrations after
ingestion of GH and CS were always below 0.5 ppm such that a clear effect of forage type could be
shown. It is questionable whether N2 O can be formed directly in the rumen under certain conditions.
Kaspar and Tiedje [45] detected traces of N2 O (up to 0.3% of added nitrogen) when investigating
the dissimilatory reduction of nitrate and nitrite by the rumen microbiota of a rumen-cannulated
cow. They concluded that N2 O is a by-product of dissimilatory nitrite reduction to ammonium rather
than a product of denitrification which seems to be absent from the rumen habitat. However, only
traces were found under those experimental feeding conditions with addition of nitrate. Also de
Raphélis-Soissan et al. [46] and Lee et al. [11] fed nitrate to ruminants in an attempt to lower ruminal
CH4 production. In this regard, two main possibilities by which NO3 − reduces enteric CH4 production
were discussed [11]: NO3 − reduction (thermodynamically favorable in comparison to methanogenesis)
as major pathway and secondly, possibly being quantitatively less important, NO3 − and NO2 − being
toxic to methanogens in the rumen. In both cases, CH4 production was decreased by addition of
nitrate, however, de Raphélis-Soissan et al. [46] stated that, on the other hand, the N2 O emission from

218
Sustainability 2018, 10, 3679

sheep in respiration chambers was increased which led to a reduction of the net benefit of methane
mitigation on global warming potential (CO2 equivalents/kg DMI) of 18%. This effect could be
mitigated by using encapsulated NO3 − as slow-release form, thereby lowering NO2 − toxicity after
nitrate ingestion [11]. When ruminants are fed typical rations without added nitrate, formation of N2 O
under anaerobic conditions in the rumen seems unlikely such that oral ways of formation after dietary
nitrate supplementation were discussed as possible mechanisms based on measurements of N2 O from
dairy cows in respiration chambers [20]. A release from the rumen via eructation was excluded by the
authors as there was no relationship at all between CH4 and N2 O in ventilation air of the respiration
chamber. However, the possibility of N2 O formation in the oral cavity can be excluded for the current
study as the gas samples were taken directly from the rumen atmosphere without oral contact. Also,
feces as a possible source of N2 O as discussed for sheep [46] can be excluded in our study due to the
sampling method. As enteric formation under anaerobic conditions seems unlikely, the transfer from
the forage into the rumen is the most likely way. In our study the AS emitted considerably more N2 O
than the other forage types. After ingestion of AS, solved N2 O may have gassed out in the rumen,
which would explain the increased concentrations in the rumen gas sample 180 min after initiation of
feed intake.
Also, the CH4 concentrations in the rumen gas sample were influenced by forage type and the
lowest concentrations were detected after ingestion of CS. In contrast to N2 O methane is formed in
the rumen as a product of carbohydrate fermentation, and the total amount is influenced by DMI
and chemical composition of the feedstuff [8] as well as by the rumen microbial community (species,
abundance, and activity of microbes) and fermentation pathways [47]. An effect of diurnal variation
on rumen CH4 concentrations as described by Bjerg et al. [48] can be excluded due to the experimental
design. A decreased concentration is not necessarily connected with a decreased total CH4 formation;
however, a reduced formation of CH4 in the rumen of cattle fed CS in comparison to other forage types
has also been observed in other studies [9] and is related to the increased propionate to acetate ratio
and a decreased rumen pH caused by feedstuffs with enhanced degradability (e.g., increased starch
and reduced fiber concentration like CS in the present study) [4,49].
The CO2 concentration in rumen gas samples was greatest after ingestion of GH and did not
differ for CS and AS, and all concentrations were in the range of values summarized from several
feeding trials [50]. The CH4 to CO2 ratio was lower for CS and GH than for AS. The lower ratio seems
to be caused by the lower CH4 concentration for CS as discussed before and an increased share of
CO2 for GH where DMI was highest. As the amount of consumed DM and its fermentability are the
main factors influencing the CO2 production [31] the amount of ingested fermentable substrate might
explain the higher CO2 concentration for GH. The CH4 to CO2 ratio can be seen as an indicator of
the efficiency of microbial fermentation as it directly describes the share of emitted C that has not
been metabolized to CO2 [31]. According to this, the efficiency of microbial fermentation was lowest
for AS. As the DMI was lowest for AS, a reduced passage rate of the digesta could have caused an
increased methanogenesis. McAllister et al. [8] concluded from several studies that properties of
forages decreasing the rate of digestion or prolonging the time of feed particles being in the rumen
generally lead to a rise in the amount of CH4 that is formed per unit of forage digested. In contrast,
recent work by Dittmann et al. [51] carefully proposed the opposite way as the CH4 production itself
might influence digesta retention in the sense of a feedback mechanism to mitigate CH4 losses by
decreasing retention time at higher CH4 production.

5. Conclusions
The experimental setup in this study with very diverging types of forages and a 3 × 3 Latin
square design made it possible to assign gaseous emissions from steers to animal- or feed-related
origin. Results indicate that fermented forages rich in CP or nitrate like alfalfa silage can release
climate-relevant N2 O with the conditions of its formation, emitting amounts and strategies for
reduction (e.g., targeted use of silage additives, feed-out management) warranting further research.

219
Sustainability 2018, 10, 3679

Under the aspect of mitigating GHG emissions from animal production also the feeding management
of farms has to be considered. The N2 O detected in the rumen gas of the steers seems to originate
from the consumed feedstuff and is probably not synthesized in the rumen. Additional studies, e.g.,
with high-yielding dairy cows and concurrent analyses of feedstuffs and environmental conditions are
needed to make those findings applicable for ruminants in general.

Author Contributions: Conceptualization, K.G., W.B. and K.-H.S.; Data curation, A.C.H.S. and M.T.; Investigation,
K.G.; Methodology, A.J.S., A.C.H.S. and M.T.; Project administration, W.B. and K.-H.S.; Supervision, K.-H.S.;
Validation, M.T.; Visualization, A.J.S.; Writing—Original draft, K.G.; Writing—Review & editing, A.J.S., M.T. and
K.-H.S.
Funding: This work was partially funded by the German Research Foundation (DFG, BU 1235/8-1, Germany).
Acknowledgments: The authors thank the staff of the Educational and Research Center Frankenforst for support
in conducting the experiments. Furthermore, this study was partly conducted by members of the Center of
Integrated Dairy Research (CIDRe), University of Bonn (Bonn, Germany).
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Gerber, P.J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling
Climate Change through Livestock: A Global Assessment of Emissions and Mitigation Opportunities; Food and
Agriculture Organization of the United Nations (FAO): Rome, Italy, 2013.
2. Hristov, A.; Oh, J.; Lee, C.; Meinen, R.; Montes, F.; Ott, T.; Firkins, J.; Rotz, A.; Dell, C.; Adesogan, A. Mitigation
of Greenhouse gas Emissions in Livestock Production: A Review of Technical Options for Non-CO2 Emissions; FAO
Anim. Produon and Health Paper; FAO: Rome, Italy, 2013; Volume 177, pp. 1–206.
3. IPCC. The Physical Science Basis. Contribution of working group I to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK, 2007.
4. McAllister, T.; Newbold, C. Redirecting rumen fermentation to reduce methanogenesis. Aust. J. Exp. Agric.
2008, 48, 7–13. [CrossRef]
5. Johnson, K.A.; Johnson, D.E. Methane emissions from cattle. J. Anim. Sci. 1995, 73, 2483–2492. [CrossRef]
[PubMed]
6. Jentsch, W.; Schweigel, M.; Weissbach, F.; Scholze, H.; Pitroff, W.; Derno, M. Methane production in cattle
calculated by the nutrient composition of the diet. Arch. Anim. Nutr. 2007, 61, 10–19. [CrossRef] [PubMed]
7. Kirchgessner, M.; Windisch, W.; Müller, H.L. Nutritional Factors for the Quantification of Methane
Production. In Proceedings of the 8th Symposium on Ruminant Physiology, 1995; Engelhart, W.,
Leonhard-Marek, S., Breves, G., Giesecke, D., Eds.; Ferdinand Enke: Stuttgart, Germany, 1995; pp. 333–348.
8. McAllister, T.; Cheng, K.-J.; Okine, E.; Mathison, G. Dietary, environmental and microbiological aspects of
methane production in ruminants. Can. J. Anim. Sci. 1996, 76, 231–243. [CrossRef]
9. Eckard, R.J.; Grainger, C.; de Klein, C.A.M. Options for the abatement of methane and nitrous oxide from
ruminant production: A review. Livest. Sci. 2010, 130, 47–56. [CrossRef]
10. Prusty, S.; Sontakke, U.; Kundu, S. Methane and nitrous oxide emission from livestock manure.
Afr. J. Biotechnol. 2014, 13, 4200–4207.
11. Lee, C.; Araujo, R.C.; Koenig, K.M.; Beauchemin, K.A. In situ and in vitro evaluations of a slow release form
of nitrate for ruminants: Nitrate release rate, rumen nitrate metabolism and the production of methane,
hydrogen, and nitrous oxide. Anim. Feed Sci. Technol. 2017, 231, 97–106. [CrossRef]
12. Macome, F.M.; Pellikaan, W.F.; Schonewille, J.T.; Bannink, A.; van Laar, H.; Hendriks, W.H.; Warner, D.;
Cone, J.W. In vitro rumen gas and methane production of grass silages differing in plant maturity and
nitrogen fertilisation, compared to in vivo enteric methane production. Anim. Feed Sci. Technol. 2017, 230,
96–102. [CrossRef]
13. Hippenstiel, F.; Pries, M.; Büscher, W.; Südekum, K.-H. Comparative evaluation of equations predicting
methane production of dairy cattle from feed characteristics. Arch. Anim. Nutr. 2013, 67, 279–288. [CrossRef]
[PubMed]
14. Storm, I.M.L.D.; Hellwing, A.L.F.; Nielsen, N.I.; Madsen, J. Methods for measuring and estimating methane
emission from ruminants. Animals 2012, 2, 160–183. [CrossRef] [PubMed]

220
Sustainability 2018, 10, 3679

15. Fernández, C.; López, M.; Lachica, M. Low-cost mobile open-circuit hood system for measuring gas exchange
in small ruminants: From manual to automatic recording. J. Agric. Sci. 2015, 153, 1302–1309. [CrossRef]
16. Place, S.E.; Pan, Y.; Zhao, Y.; Mitloehner, F.M. Construction and operation of a ventilated hood system for
measuring greenhouse gas and volatile organic compound emissions from cattle. Animals 2011, 1, 433–446.
[CrossRef] [PubMed]
17. Hassanat, F.; Gervais, R.; Julien, C.; Massé, D.I.; Lettat, A.; Chouinard, P.Y.; Petit, H.V.; Benchaar, C. Replacing
alfalfa silage with corn silage in dairy cow diets: Effects on enteric methane production, ruminal fermentation,
digestion, N balance, and milk production. J. Dairy Sci. 2013, 96, 4553–4567. [CrossRef] [PubMed]
18. Haque, M.N.; Hansen, H.H.; Storm, I.M.; Madsen, J. Comparative methane estimation from cattle based on
total CO2 production using different techniques. Anim. Nutr. 2017, 3, 175–179. [CrossRef] [PubMed]
19. Rotz, C.A.; Thoma, G. Assessing carbon footprints of dairy production systems. In Large Dairy Herd
Management, 3rd. ed.; Beede, D.K., Ed.; American Dairy Science Association: Champaign, IL, USA, 2017;
pp. 19–31.
20. Petersen, S.O.; Hellwing, A.L.F.; Brask, M.; Højberg, O.; Poulsen, M.; Zhu, Z.; Baral, K.R.; Lund, P. Dietary
nitrate for methane mitigation leads to nitrous oxide emissions from dairy cows. J. Environ. Qual. 2015, 44,
1063–1070. [CrossRef] [PubMed]
21. Emery, I.; Mosier, N. Direct emission of methane and nitrous oxide from switchgrass and corn stover:
Implications for large-scale biomass storage. GCB Bioenergy 2015, 7, 865–876. [CrossRef]
22. Wang, L.C.; Burris, R. Toxic gases in silage, mass spectrometric study of nitrogenous gases produced by
silage. J. Agric. Food Chem. 1960, 8, 239–242. [CrossRef]
23. Spoelstra, S.F. Nitrate in silage. Grass Forage Sci. 1985, 40, 1–11. [CrossRef]
24. Pahlow, G.; Muck, R.E.; Driehuis, F.; Oude Elferink, S.J.W.H.; Spoelstra, S.F. Microbiology of ensiling.
In Silage Science and Technology; Buxton, D.R., Muck, R.E., Harrison, J.H., Eds.; ASA, CSSA, SSSA: Madison,
WI, USA, 2003; pp. 31–93.
25. Zhao, Y.; Wexler, A.S.; Hase, F.; Pan, Y.; Mitloehner, F.M. Detecting nitrous oxide in complex mixtures using
FTIR spectroscopy: Silage gas. J. Environ. Prot. 2016, 7, 1719–1729. [CrossRef]
26. Franco, R. Measuring Emissions and Developing Strategies to Mitigate Volatile Organic Compounds and
Oxides of Nitrogen from Silage. Ph.D. Thesis, University of California, Davis, CA, USA, 2016.
27. Schmithausen, A.J.; Trimborn, M.; Büscher, W. Sources of nitrous oxide and other climate relevant gases on
surface area in a dairy free stall barn with solid floor and outside slurry storage. Atmos. Environ. 2018, 178,
41–48. [CrossRef]
28. Wulf, S.; Maeting, M.; Clemens, J. Application technique and slurry co-fermentation effects on ammonia,
nitrous oxide, and methane emissions after spreading. J. Environ. Qual. 2002, 31, 1795–1801. [CrossRef]
[PubMed]
29. Clemens, J.; Trimborn, M.; Weiland, P.; Amon, B. Mitigation of greenhouse gas emissions by anaerobic
digestion of cattle slurry. Agric. Ecosyst. Environ. 2006, 112, 171–177. [CrossRef]
30. Schmithausen, A.J.; Trimborn, M.; Büscher, W. Methodological comparison between a novel automatic
sampling system for gas chromatography versus photoacoustic spectroscopy for measuring greenhouse gas
emissions under field conditions. Sensors 2016, 16, 1638. [CrossRef] [PubMed]
31. Madsen, J.; Bjerg, B.S.; Hvelplund, T.; Weisbjerg, M.R.; Lund, P. Methane and carbon dioxide ratio in excreted
air for quantification of the methane production from ruminants. Livest. Sci. 2010, 129, 223–227. [CrossRef]
32. Weißbach, F.; Strubelt, C. Correcting the dry matter content of grass silages as a substrate for biogas
production. Landtechnik 2008, 63, 210–246.
33. Weißbach, F.; Strubelt, C. Correcting the dry matter content of maize silages as a substrate for biogas
production. Landtechnik 2008, 63, 82–83.
34. VDLUFA. VDLUFA-Methodenbuch, Bd. III. Die Chemische Untersuchung von Futtermitteln; VDLUFA-Verlag:
Darmstadt, Germany, 2012.
35. Brandt, M.; Schuldt, A.; Mannerkorpi, P.; Vearasilp, T. Zur enzymatischen Stärkebestimmung im Darminhalt
und Kot von Kühen mit hitzestabiler Amylase. Arch. Anim. Nutr. 1987, 37, 455.
36. Menke, K.H.; Steingass, H. Schätzung des energetischen Futterwerts aus der in vitro mit Pansensaft
bestimmten Gasbildung und der chemischen Analyse. II. Regressionsgleichungen. Übers Tierernährg 1987,
15, 59–94.

221
Sustainability 2018, 10, 3679

37. GfE. Equations for predicting metabolisable energy and digestibility of organic matter in forage legumes for
ruminants. Proc. Soc. Nutr. Physiol. 2017, 26, 186–193.
38. GfE. New equations for predicting metabolisable energy of grass and maize products for ruminants. Proc. Soc.
Nutr. Physiol. 2008, 17, 191–197.
39. Weiß, K.; Kaiser, E. Milchsäurebestimmung in Silageextrakten mit Hilfe der HPLC. Wirtschaftseig. Futter
1995, 41, 69–80.
40. von Lengerken, J.; Zimmermann, K. Handbuch Futtermittelprüfung; Deutscher Landwirtschaftsverlag: Berlin,
Germany, 1991.
41. Barry, T.; Thompson, A.; Armstrong, D. Rumen fermentation studies on two contrasting diets. 1. Some
characteristics of the in vivo fermentation, with special reference to the composition of the gas phase,
oxidation/reduction state and volatile fatty acid proportions. J. Agric. Sci. 1977, 89, 183–195. [CrossRef]
42. Lindgren, S.; Pettersson, K.; Kaspersson, A.; Jonsson, A.; Lingvall, P. Microbial dynamics during aerobic
deterioration of silages. J. Sci. Food Agric. 1985, 36, 765–774. [CrossRef]
43. McAllister, T.A.; Feniuk, R.; Mir, Z.; Mir, P.; Selinger, L.B.; Cheng, K.J. Inoculants for alfalfa silage: Effects
on aerobic stability, digestibility and the growth performance of feedlot steers. Livest. Prod. Sci. 1998, 53,
171–181. [CrossRef]
44. Weinberg, Z.G.; Ashbell, G. Changes in gas composition in corn silages in bunker silos during storage and
feedout. Can. Agric. Eng. 1994, 36, 155–158.
45. Kaspar, H.F.; Tiedje, J.M. Dissimilatory reduction of nitrate and nitrite in the bovine rumen: Nitrous oxide
production and effect of acetylene. Appl. Environ. Microbiol. 1981, 41, 705–709. [PubMed]
46. De Raphélis-Soissan, V.; Li, L.; Godwin, I.R.; Barnett, M.C.; Perdok, H.B.; Hegarty, R.S. Use of nitrate and
Propionibacterium acidipropionici to reduce methane emissions and increase wool growth of Merino sheep.
Anim. Prod. Sci. 2014, 54, 1860–1866. [CrossRef]
47. Knapp, J.R.; Laur, G.L.; Vadas, P.A.; Weiss, W.P.; Tricarico, J.M. Invited review: Enteric methane in dairy
cattle production: Quantifying the opportunities and impact of reducing emissions. J. Dairy Sci. 2014, 97,
3231–3261. [CrossRef] [PubMed]
48. Bjerg, B.; Zhang, G.; Madsen, J.; Rom, H.B. Methane emission from naturally ventilated livestock buildings
can be determined from gas concentration measurements. Environ. Monit. Assess. 2012, 184, 5989–6000.
[CrossRef] [PubMed]
49. Beauchemin, K.A.; Kreuzer, M.; O’Mara, F.; McAllister, T.A. Nutritional management for enteric methane
abatement: A review. Aust. J. Exp. Agric. 2008, 48, 21–27. [CrossRef]
50. Hegarty, R.; Gerdes, R. Hydrogen production and transfer in the rumen. Rec. Adv. Anim. Nutr. Aust. 1999,
12, 37–44.
51. Dittmann, M.T.; Hammond, K.J.; Kirton, P.; Humphries, D.J.; Crompton, L.A.; Ortmann, S.; Misselbrook, T.H.;
Südekum, K.-H.; Schwarm, A.; Kreuzer, M.; et al. Influence of ruminal methane on digesta retention and
digestive physiology in non-lactating dairy cattle. Br. J. Nutr. 2016, 116, 763–773. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

222
 sustainability

Article
Assessing the Greenhouse Gas Mitigation Effect of
Removing Bovine Trypanosomiasis in Eastern Africa
Michael MacLeod 1, *, Vera Eory 1 ID , William Wint 2 , Alexandra Shaw 3 , Pierre J. Gerber 4,5 ,
Giuliano Cecchi 6 ID , Raffaele Mattioli 7 , Alasdair Sykes 1 and Timothy Robinson 7
1 Land Economy, Environment and Society Group, SRUC, Edinburgh EH9 3JG, UK;
[email protected] (V.E.); [email protected] (A.S.)
2 Department of Zoology, Environmental Research Group Oxford (ERGO), South Parks Road,
Oxford OX1 3PS, UK; [email protected]
3 AP Consultants, 22 Walworth Enterprise Centre, Duke Close, Andover SP10 5AP, UK;
[email protected]
4 The World Bank Group, Agriculture and Food Global Practice, 1818 H Street N.W.,
Washington, DC 20433, USA; [email protected]
5 Animal Production Systems Group, Wageningen University, P.O. Box 338, Wageningen 6708, The Netherlands
6 Food and Agriculture Organization of the United Nations (FAO), Sub-regional Office for Eastern Africa,
CMC Road, P.O. Box 5536, Addis Ababa, Ethiopia; [email protected]
7 Food and Agriculture Organization of the United Nations (FAO), Animal Production and Health Division,
Viale delle Terme di Caracalla, 00153 Rome, Italy; [email protected] (R.M.);
[email protected] (T.R.)
* Correspondence: [email protected]; Tel.: +44-131-535-4124

Received: 25 April 2018; Accepted: 15 May 2018; Published: 18 May 2018

Abstract: Increasing the production of meat and milk within sub-Saharan Africa should provide
significant food security benefits. However, greenhouse gas (GHG) emissions represent a challenge,
as cattle production in the region typically has high emissions intensity (EI), i.e., high rates of GHG
emissions per unit of output. The high EI is caused by the relatively low production efficiencies in the
region, which are in turn partly due to endemic cattle diseases. In theory, improved disease control
should increase the efficiency and decrease the emissions intensity of livestock production; however
quantitative analysis of the potential GHG mitigation effects of improved disease control in Africa is
lacking. This paper seeks to respond to this by using a hybrid modelling approach to quantify the
production and emissions effects of removing trypanosomiasis from East African cattle production
systems. The emissions are quantified for each cattle production system using an excel version of
GLEAM, the Food and Agriculture Organization’s Global Livestock Environmental Assessment
Model. The results indicate that removing trypanosomiasis leads to a reduction in the emissions
intensity per unit of protein produced of between 0% and 8%, driven mainly by the increases in
milk yields and cow fertility rates. Despite the limitations, it is argued that the approach provides
considerable scope for modelling the GHG impacts of disease interventions.

Keywords: cattle health; climate change; livestock modelling; GLEAM; sustainable intensification

1. Introduction
In developing countries growing populations, rising incomes, and urbanization are translating
into increasing demand for livestock products. Livestock is now one of the fastest growing sub-sectors
of agriculture: a doubling of demand for animal-source foods is expected within developing countries
between 2000 and 2050, and a 70% increase for the world as a whole [1,2]. However, it has been noted
that: “Meeting this demand in a way that is socially desirable and environmentally sustainable is a
major challenge facing agriculture today” [3] (p. 9).

Sustainability 2018, 10, 1633; doi:10.3390/su10051633 223 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 1633

A major part of the challenge is the emission of greenhouse gases (GHGs) arising from livestock
production. It has been estimated through life-cycle assessments that the global livestock sector
accounts for around 14.5% of all anthropogenic GHG emissions, with cattle meat and milk accounting
for 65% of the livestock emissions [4]. If increased demand is to be met without significant increases in
GHG emissions, then ways of reducing the emissions intensity (EI, i.e., the amount of GHG emitted
per unit of commodity produced) need to be identified and deployed.
Improving livestock health is potentially a cost-effective way of increasing production,
while reducing EI. The World Organisation for Animal Health (OIE) has estimated that: “at the
worldwide level, average losses due to animal diseases are more than 20%” [5]. The main direct
farm level losses arise from mortality (including involuntary culling), a lowering of the efficiency
of the production process, and reduction in output quantity or quality [6]. Reducing the disease
burden can lead to significant reductions in EI by, for example, improving the feed conversion ratio
of individual animals or changing herd structures (i.e., the proportion of each animal cohort in the
herd). However, disease reduction is not yet widely recognised as a mitigation measure [7]. In fact,
the Intergovernmental Panel on Climate Change Fifth Assessment Report [8] does not specifically
mention livestock health, and current evidence is limited to a small number of studies of European
livestock [9–13].
Understanding the impacts of improving cattle health on production and emissions is of particular
relevance in sub-Saharan Africa (SSA), given that cattle are the predominant source of livestock
GHGs [4], growth in demand between 2000 and 2030 is forecast to be 113% for beef and 107% for dairy
products [1] and that the EIs for bovine milk and meat tend to be higher in SSA than in other regions [14].
The higher EIs are largely due to inefficiencies in converting natural resources into edible animal
products, with relatively high feed conversion ratios and high energy (methane) and nitrogen (nitrous
oxide) losses occurring along the process [4]. In these systems, efficiency is closely and positively
related to productivity and key factors such as: milk yield, growth rates, fertility and mortality
rates, and ages at slaughter. These, in turn, are a function of the genetics, feeding, management,
environmental stress, and health status of the animals.
While various studies have investigated the effects of improved genetics, feeding, and management
on livestock [15], evidence on the mitigation potential of improving health is scarce. It has been noted
that, “Simulation results seem promising, but reliable quantitative estimates of the mitigation potential
of improved health will require more research” [16] (p. 111). This paper seeks to respond to this by
using a hybrid modelling approach to quantify the production and emissions effects of removing
trypanosomiasis from East African cattle systems.
Trypanosomiasis is a disease caused by tsetse-transmitted parasitic protozoans, and is endemic in
a tsetse-infested belt that spans across 9 million square kilometres in SSA [17]. With its animal form
(called “nagana”) and its human form (also known as “sleeping sickness”), trypanosomiasis is widely
considered as one of the main threats to human and livestock health and agricultural production,
and, as such, a major constraint to rural development and poverty alleviation in SSA [18,19]. It has
been identified as “the most economically important disease of livestock in sub-Saharan Africa” [20].
African trypanosomiasis, in its various forms, can cause a wide range of symptoms, including anaemia,
wasting, loss of condition, abortion, and reduced milk production. Progression can lead either to death
or to a chronic form. For many decades chemotherapy has been the mainstay of trypanosomiasis
control, but in recent years resistance has emerged as a growing concern [21].
This paper presents a method for quantifying the effect of trypanosomiasis treatment on the
production and EI of a range of cattle production systems. It quantifies the effect of trypanosomiasis
treatment on the EI in East Africa. The limitations of the method are discussed and the wider challenges
in quantifying the GHG effects of livestock health improvement are explored.

224
Sustainability 2018, 10, 1633

2. Materials and Methods

2.1. Study Area

The study focuses on East Africa, which is one of the most important dairy development zones in
SSA. The specific area of study is the Inter-Governmental Authority on Development (IGAD) region,
an area of over 5.2 million km2 that comprises the countries of Djibouti, Eritrea, Ethiopia, Kenya,
Somalia, South Sudan, Sudan, and Uganda [22]. Just under half (45%) of the cattle in SSA are reported
to be in the IGAD region [23].

2.2. Cattle Production Systems

The cattle in the study area were classified into twelve distinct production systems (Table 1).
These refined cattle systems were based on three main livestock systems (i.e., pastoral, agro-pastoral
and mixed farming) [24], which were further disaggregated based on the prevalence of work oxen
(used for traction) and milk yields of dairy cattle (which have varying degrees of exotic genetic material,
usually of the main European dairy breeds that have been widely adopted in high value smallholder
dairy production in Eastern Africa).

Table 1. The 12 cattle production systems analysed, table adapted from [25].

Production System
Draft Oxen Mixed: Mixed: High Milk
Pastoral Agro-Pastoral
General a Ethiopia a Yield Dairy
No oxen ×× b
Low oxen × × × ×
Medium oxen × × ×
High oxen × × ×
a Two mixed farming systems were analysed, one for Ethiopia and one for the other study countries; b High milk

yield dairy cows are found in the agro-pastoral and general mixed farming systems.

The high milk yield dairy systems consist of cattle with varying degrees of non-indigenous genetic
material derived primarily from the main European dairy breeds, principally Ayrshire, Friesian and
Channel Island breeds—Guernsey and Jersey. In the other systems indigenous breeds predominate,
i.e., zebu cattle and related crossbreeds [26]. The eastern African indigenous zebu cattle breeds are
conventionally divided into three main groups all of which are represented in the countries covered
by this study: the Large East African Zebu (including the Boran breeds of Ethiopia, Kenya and
Somalia, the Samburu, Karmajong Zebu, Orma Boran and Butana and Kenana of Sudan) the Small East
African Zebu (including the Maasai, Abyssinian Shorthorned Zebu, Kamba of Kenya and Serere and
Kyoga in the tsetse-infested areas of Uganda) and the Sanga cattle (including the Ankole of Uganda,
Danakil cattle of Ethiopia and the Nuer and Dinka of Sudan). Further information is available on the
Domestic Animal Genetic Resources Information System (DAGRIS) [27]. More detail on the production
systems and how they were defined is available in [28].
Data on the use of work oxen were obtained from in-country informants, reports, census data,
livelihood studies [24] and other sources [29–33]. Combining these sources across the region by
administrative area, and studying data on herd compositions, enabled three broad categories of oxen
use to be distinguished depending on the proportion of cattle used for draught: low (≤10%), medium
(>10% and <20%), and high (≥20%).
The proportion of cattle modelled in each system is given in Table 2. The most recent statistics
report a total cattle population in the study area of 144.5m in 2016 [23].

225
Sustainability 2018, 10, 1633

Table 2. The proportion of cattle in each system.

Production System % of Total Cattle Population

Pastoral 12%
Agropastoral, low dairy and oxen 34%
Mixed, low dairy and oxen 11%
Agropastoral, high dairy and low oxen 2%
Agropastoral, low dairy and medium oxen 1%
Agropastoral, low dairy and high oxen 2%
Mixed, high dairy and low oxen 4%
Mixed, low dairy and low oxen 1%
Mixed, low dairy and high oxen 1%
Mixed, low dairy and medium oxen (eth) 7%
Mixed, low dairy and high oxen (eth) 18%
Mixed, low dairy and low oxen (eth) 8%
Total 100%

2.3. Modelling Approach

This study builds on previous work, which quantified the economic benefits of removing
trypanosomiasis in East African cattle using the “Mapping the Benefits” (MTB) model [25,28,34].
In this study, the MTB model is combined with an excel version of GLEAM (the UN-FAO’s Global
Livestock Environmental Assessment Model, [35]) which calculates the GHG emissions arising from
production. A schematic diagram of the relationship between the models is provided in Figure 1.

Figure 1. Schematic diagram of the relationship between the two models: Mapping the Benefits (MTB)
and Global Livestock Environmental Assessment Model (GLEAM).

2.3.1. Harmonising the GLEAM and MTB Herd Models

At the heart of both GLEAM and MTB are herd models, which determine the herd structure and
the number of animals entering and leaving the herd each year. The two herd models perform some of
these calculations in different ways. For example, they have different animal cohorts (adult female,
replacement female, etc.) and different ways of calculating the number of calves born. Therefore,
the herd models had to be harmonised, i.e. adjusted until they produced the same herd structure and
dynamics. This was achieved by comparing the results given by the two herd models with the same
input data, and adjusting the calculations in GLEAM until the models were producing the same results
for all 12 production systems.

226
Sustainability 2018, 10, 1633

2.3.2. Estimating the Effects of Trypanosomiasis Treatment over 20 Years

The herd structure and dynamics, and the output of meat and milk were calculated for the
situations with and without trypanosomiasis using the MTB model [34] and applied to cattle population
density maps, projected using the herd growth and additional spread models. Regional tsetse maps at
1 km resolution were used [36], complemented by 5km resolution continental datasets [37] where 1 km
resolution maps were unavailable. Cattle population densities were available from a series of 1km
resolution datasets created within the framework of the IGAD Land Policy Initiative (LPI) using the
most recent national statistics available for the period 2000–2005. The mapping methods were those
developed to generate the Gridded Livestock of the World [38].
GLEAM was used to calculate the (meat and milk) production, the total greenhouse gas emissions
arising from that production and the EI of each commodity for each of the cattle systems with and
without trypanosomiasis. The meat production in live weight was calculated by multiplying the
number of cattle exiting the herd as offtake, i.e., sold or slaughtered, by the average live weight of
each cohort (i.e., adult female, calves etc.). The live weight was then converted to edible protein by
multiplying it by (a) the carcass weight: live weight percentage (50–55% depending on the cohort);
(b) the bone-free meat: carcass weight percentage (75%) and finally (c) the protein content of bone-free
meat (18%). The edible protein from milk was determined by multiplying the net milk production
(milk secreted minus milk suckled) by the protein content of milk (3.3%). Emissions are only allocated
to edible protein and draft, however cattle perform other functions. It has been estimated that 16%
of the emissions should be allocated to the manure, financing and dowry functions of cattle [39].
Doing so would reduce the EI but would have a negligible impact on the change in EI arising from
trypanosomiasis removal.
The main GHG-producing activities were included, i.e., the production of feed and fertiliser,
the digestion of feed and the excretion of undigested organic matter (Table 3 provides an explanation
of the emission categories). The emissions of methane and nitrous oxide were converted to their carbon
dioxide equivalent using the Intergovernmental Panel on Climate Change (IPCC) global warming
potentials of 25 and 298, respectively. The system boundary of the study is “cradle to farm-gate”,
i.e., emissions arising from the production of feed and other inputs are included but post-farm gate
emissions occurring during processing and distribution are not included; however in the systems
studied post-farm gate emissions are likely to represent a small proportion of the total emissions [4].
CO2 emissions and sequestration in short-term carbon cycles (i.e., respiration and photosynthesis)
are not included, in keeping with the IPCC guidelines ([40], Volume 4, p. 10.7). Furthermore, it is
assumed that the treatment (chemotherapy) has negligible additional GHG emissions arising (from
drug manufacture and distribution) given the small doses involved. Other treatment strategies, such as
the removal of tsetse habitats, could lead to significant additional GHG emissions.

Table 3. The emission categories quantified in the study.

Category Emissions Sources

Direct and N2 O arising from the nitrification/denitrification of excreted
Manure N2 O
N during its management and storage.
CH4 arising from the anaerobic decomposition of excreted organic
Manure CH4
matter during its management and storage.
Enteric fermentation CH4 CH4 arising from the microbial decomposition of feed during digestion.
CO2 from: fossil fuel use in the cultivation of feed crops; fossil fuel use
in the production of non-crop feed materials; processing, transportation
Feed energy CO2
and blending of feed materials; fossil fuel use from the production of
synthetic fertiliser; land use change arising from soy cultivation.
Direct and indirect N2 O from: application of synthetic fertiliser and
Feed N2 O manure to crops; crop residue management; direct deposition of N by
grazing animals; fertiliser manufacture.

227
Sustainability 2018, 10, 1633

2.3.3. Parameterising the Cattle Production Systems

The values for the baseline situation (i.e., with trypanosomiasis) in Table 4 were derived from
various sources. A few sources provided information relating to all production systems [32,41], others for
the pastoralist systems [42–44], for the agro-pastoral and mixed farming systems [29,31,45–50] and for
the high milk yield “grade” dairy cattle kept in a separate system alongside indigenous cattle in the
agro-pastoral and mixed farming systems [51–53].

Table 4. Values for selected parameters used in the analysis (T+ refers to the value with trypanosomiasis,
T− to the value without trypanosomiasis). The values were estimated based on a review of longitudinal
and cross-sectional studies comparing the productivity observed in infected and uninfected individual
cattle or whole herds, under conditions of both high and low trypanosomiasis challenge (see Section 2.3.3).
Table adapted from [25].

Cattle Production Systems

Parameter
Mixed Farming Mixed Farming High Milk Yield
Pastoral Agro-Pastoral
(General) (Ethiopia) Dairy
T+ T− T+ T− T+ T− T+ T− T+ T−
Mortality % of animals dying each year
Female calves 20 17 18 15 16 13 24 20 21 18
Male calves 25 22 20 17 18 15 26 22 26 23
Adult females 7.5 6.5 7.0 6.0 8.0 7.0 9.0 7.5 12.0 10.0
Work oxen 9.0 7.2 8.5 6.8 9.0 7.2 10.0 8.0 - -
Fertility % of cows producing a living calf each year
Cow fertility 54 58 52 56 51 55 49 54 53 57
Lactation Litres of milk per lactation a
Milk offtake 275 296 285 306 300 322 280 301 1900 2042
a Lactation length varies depending on the system; in this study it is assumed that most of the milk for human

consumption is taken off in the 12 months following calving.

The effects of trypanosomiasis treatment on performance were estimated based on a review

of longitudinal and cross-sectional studies comparing the productivity observed in infected and
uninfected individual cattle or whole herds, under conditions of both high and low trypanosomiasis
challenge [33,45,54–61]. The review gave a range of values for the effect of the disease. In this study,
it was assumed that disease treatment would have an effect between the middle and lower end of the
range reported in studies. These (arguably conservative) assumptions were made in order to correct
for the fact that the studies reviewed tended to be conducted in areas where the disease impact was
relatively severe.
Similar impacts for trypanosomiasis were applied across the production systems (Table 4).
This table also shows that baseline cattle mortality rates observed in Eastern Africa tend to be high.
This reflects not just the presence of trypanosomiasis, but also of tick-borne diseases, especially East
Coast fever [60] and, locally, very high stocking rates leading to nutritional stress, especially in parts of
the Ethiopian highlands [62].

2.3.4. Ration Composition and Nutritional Value

The ration (i.e., the livestock feed) for each system was determined using a combination of
approaches. The proportions of the main feed material categories (i.e., forage, crop residues and
concentrates) were estimated based on literature, expert knowledge, and unpublished surveys,
while the percentage of each crop residue (maize, millet and sorghum stover, wheat, rice and barley
straw, and sugar cane tops) were calculated for each cell, based on how much of each crop is produced
within the cell. Crop data was extracted for livestock production zones from Spatial Production
Allocation Model (SPAM) V3r6 2000 datasets [63]. The nutritional value of the ration was calculated by
multiplying the nutritional value of each feed material by its proportion in the ration. The nutritional

228
Sustainability 2018, 10, 1633

values of individual feed materials were based on [14,64], the Sub-Saharan Africa Feed Composition
Database [65], and Feedipedia [66,67].

2.3.5. Estimating Uncertainty

Calculation of the emission intensities involves parameters that are subject to some degree of
uncertainty. A Monte Carlo simulation was undertaken in order to quantify the uncertainty ranges
in the results. Parameters were included in the simulation that were (a) likely to have a significant
influence on the most important emissions categories (those contributing more than twenty percent
of the total emissions, i.e., enteric CH4 and feed N2 O) and (b) had a high degree of uncertainty or
inherent variability. An initial list of parameters was generated and reviewed. Based on the review,
some parameters were excluded, e.g., the emission factors (EFs) for indirect N2 O were removed because
volatilisation and leaching only account for a small % of feed N2 O emissions, and a previous study had
found the contribution to variance of these EFs to be very small (<2%) [14] (p. 81). The distributions
and variability of the parameters are given in Table 5. The variability of forage digestibility is based on
the standard deviation of the digestibility of Napier grass (Pennisetum purpureum) reported in [67].
The variability of cow milk yield, cow fertility and calf death rates were based on the ranges reported
in [32]. The Monte Carlo was performed in Model Risk with 5000 runs for each of 12 systems with and
without trypanosomiasis.

Table 5. Parameters included in the Monte Carlo analysis.

Coefficient of
Parameter Distribution Minimum-Maximum Basis
Variance
Forage digestibility, DE% Normal 6% [67]
Milk yield Normal 11–39% [32]
Cow fertility Normal 8–21% [32]
Calf death rate Normal 25–45% [32]
Enteric CH4 factor, Ym Normal 10% [40], (Vol. 4, p. 10.33)
N2 O Emission factor 1 Lognormal 0.003–0.03 [40], (Vol. 4, p. 11.11)
N2 O Emission factor 3 Lognormal 0.007–0.06 [40], (Vol. 4, p. 11.11)

3. Results

3.1. Baseline Emissions with Trypanosomiasis

The EI by system and emission category is shown in Figure 2. The main sources of emissions
are (a) enteric methane and (b) feed nitrous oxide, i.e., the nitrous oxide arising from the deposition
of organic N on pasture (either directly via the urine of grazing animals, or via the spreading of
the collected manure of housed cattle). The high (milk yield) dairy systems have much lower EI
than other systems due to their higher productivity (where productivity is defined as the mass of
meat and milk produced by a system each year compared to the live weight mass of the cattle in the
system). Differences between the other systems are less marked but also largely driven by productivity.
The relationship between productivity and EI for the 12 systems with and without trypanosomiasis is
shown in Figure 3. This trend is consistent with other studies [68,69] which found a similar relationship
between productivity and EI in cattle systems, i.e., large (but reducing) marginal decreases in EI with
increasing productivity in low productivity systems, such as those in East Africa.

229
Sustainability 2018, 10, 1633

Figure 2. Emissions intensity (EI) by cattle production system and emissions category (kgCO2 e/kg
edible protein at farm gate). AP: agro-pastoral. The errors bars show the 95% confidence intervals.

ϱϬϬ
ϰϱϬ
ϰϬϬ
;ŬŐKϮĞͬŬŐĞĚŝďůĞƉƌŽƚĞŝŶͿ

ϯϱϬ
ŵŝƐƐŝŽŶƐŝŶƚĞŶƐŝƚLJ

ϯϬϬ /сϵϯ͘ϲWͲϬ͘ϴϵ
ϮϱϬ ZϸсϬ͘ϵϵ

ϮϬϬ
ϭϱϬ
ϭϬϬ
ϱϬ
Ϭ
Ϭ͘ϬϬ Ϭ͘ϮϬ Ϭ͘ϰϬ Ϭ͘ϲϬ Ϭ͘ϴϬ ϭ͘ϬϬ ϭ͘ϮϬ
WƌŽĚƵĐƚŝǀŝƚLJ͕W;ŬŐŽĨĞĚŝďůĞƉƌŽƚĞŝŶŽƵƉƵƚƉĞƌŬŐůŝǀŝŶŐƉƌŽƚĞŝŶͿ

Figure 3. The relationship between productivity and EI for the 12 cattle production systems with and
without trypanosomiasis. Productivity is defined as the mass of meat and milk edible protein produced
by a system each year compared to the live weight mass of the cattle in the system (measured in terms
of mass of living protein).

3.2. Effect of Disease Treatment

Treatment of trypanosomiasis leads to increases in production and emissions across all the
systems. Figure 4 shows the increases once the full effects of disease treatment have been achieved.
Production increases relatively more than emissions leading to reductions in EI of 0% to 8%.

230
Sustainability 2018, 10, 1633

The reductions in EI are significant in eleven of the twelve systems and are closely (inversely) correlated
with the change in productivity (Figure 5).
ŝĨĨĞƌĞŶĐĞŝŶĞŵŝƐƐŝŽŶƐĂŶĚĞĚŝďůĞƉƌŽƚĞŝŶ;йͿ

ϮϬ
ϭϴ
ϭϲ
ϭϰ
ϭϮ
ϭϬ dŽƚĂůĞĚŝďůĞ
ϴ ƉƌŽƚĞŝŶ
ϲ
ϰ dŽƚĂů','
Ϯ ĞŵŝƐƐŝŽŶƐ
Ϭ

ĂƚƚůĞƉƌŽĚƵĐƚŝŽŶƐLJƐƚĞŵ

Figure 4. Difference in total edible protein production and GHG emissions with disease treatment.
AP: agro-pastoral.

ϭ
ŚĂŶŐĞŝŶĞŵŝƐƐŝŽŶƐŝŶƚĞŶƐŝƚLJ͕ȴ/;йͿ

ĞϮ
Ϭ
ͲϮ Ͳϭ
Ϭ Ϯ ϰ ϲ ϴ ϭϬ ϭϮ
Ğϯ ŵϯ
ͲϮ
Ăϯ
Ͳϯ ĂϮ
ŵϰ ȴ/сͲϬ͘ϲϳȴW Ͳ Ϭ͘ϵ
Ăϰ Ɖ
Ͳϰ ZϸсϬ͘ϵϴ
Ͳϱ Ğϭ

Ͳϲ ŵϮ
Ͳϳ
Ͳϴ
Ăϭ ŵϭ
Ͳϵ
ŚĂŶŐĞŝŶƉƌŽĚƵĐƚŝǀŝƚLJ͕ȴW;йͿ

Figure 5. Change in EI and productivity with disease treatment. EI is measured in terms of kgCO2 e
per kg of edible protein produced and productivity. Productivity is defined as the mass of meat and
milk edible protein produced by a system each year compared to the live weight mass of the cattle
in the system (measured in terms of mass of living protein). (Key: a1 = agro-pastoral high dairy;
a2 = agro-pastoral low dairy, high oxen; a3 = agro-pastoral low dairy, medium oxen; a4 = agro-pastoral
low dairy, low oxen; m1 = mixed high dairy; m2 = mixed low dairy, high oxen; m3 = mixed low dairy,
medium oxen; m4 = mixed, low dairy, low oxen; e1 = Ethiopia low dairy, high oxen; e2 = Ethiopia low
dairy, medium oxen; e3 = Ethiopia, low dairy, low oxen; p = pastoral.).

231
Sustainability 2018, 10, 1633

3.3. Factors driving the Changes in EI

A sensitivity analysis was undertaken in order to investigate the influence of different parameters
on EI (Table 6). The EI is highly sensitive to changes in the digestibility of forage, and to the enteric
methane emission factor (Ym), however, both of these remain constant with changes in disease status.
Increased milk yield leads to a decrease in EI as a greater percentage of the lactating cow’s feed energy
requirement is used for the production of edible outputs (i.e., lactation) rather than non-productive
activity (e.g., maintenance or locomotion), [68]. The increased cow fertility rate leads to a higher
proportion of the adult females producing edible outputs. This is important as while non-lactating
adult females produce lower emissions than lactating ones, they produce no edible outputs (i.e., milk
or liveweight gain) so their EI is effectively infinite. The increased fertility rate also changes the
herd structure, but this has a limited effect on EI. EI is less sensitive to changes in calf mortality
than it is to changes in cow milk yield or fertility, however the effect of calf mortality on EI depends
on the fate of the dying calves, i.e., what proportion enter the human food chain and are therefore
counted as production. Finally, increasing the use of draft oxen leads to increases EI in some systems.
Draft animals have a high EI as they produce no/limited edible output, so even when a proportion of
the emissions are allocated to labour, they still have a higher EI than younger, faster growing cattle.

Table 6. Summary of the sensitivity analysis, showing the change in EI resulting from a ±10% change
in each parameter (“Draft”: the % of male cattle aged >3 years old that are used for draft. EF: emission
factor; DE: digestible energy).

Change in EI

System Change in Constant Vary with System Vary with System and Disease Status
Parameter
N2 O N2 O Forage Enteric Milk Cow Calf Death
Draft
EF1 EF3 DE% CH4 , Ym Yield Fertility Rate
Pastoral +10% 0.7% 1.2% −16.4% 7.2% −4.5% −3.9% −0.6% 0.5%
Pastoral −10% −0.7% −1.2% 23.1% −7.2% 4.9% 4.9% 0.6% −0.5%
AP, high dairy +10% 1.6% 0.1% −15.8% 5.1% −6.3% −5.4% 2.2% 0.0%
AP, high dairy −10% −1.6% −0.1% 22.2% −5.1% 7.5% 6.7% 0.0% 0.0%
AP, low oxen +10% 1.4% 0.7% −16.4% 6.3% −4.4% −2.9% −0.7% 1.0%
AP, low oxen −10% −1.4% −0.7% 23.5% −6.3% 4.8% 3.5% 0.7% −1.0%
AP, medium oxen +10% 1.1% 0.7% −16.5% 6.8% −4.4% −3.0% −0.7% 2.0%
AP, medium oxen −10% −1.1% −0.7% 23.7% −6.8% 4.8% 3.6% 0.7% −2.0%
AP, high oxen +10% 1.3% 0.7% −16.3% 6.5% −4.4% −3.1% −0.7% 3.8%
AP, high oxen −10% −1.3% −0.7% 23.3% −6.5% 4.9% 3.9% 0.7% −3.8%
Mixed, high dairy +10% 1.6% 0.1% −15.8% 5.1% −6.3% −5.4% 2.3% 0.0%
Mixed, high dairy −10% −1.6% −0.1% 22.2% −5.1% 7.5% 6.7% −0.1% 0.0%
Mixed, low oxen +10% 1.2% 0.3% −17.1% 6.7% −4.4% −1.7% −0.9% 0.9%
Mixed, low oxen −10% −1.2% −0.3% 24.9% −6.7% 4.9% 2.0% 0.9% −0.9%
Mixed, medium oxen +10% 1.8% 0.3% −16.7% 6.2% −4.5% −2.7% −0.6% 2.0%
Mixed, medium oxen −10% −1.8% −0.3% 24.1% −6.2% 4.9% 3.7% 0.6% −2.0%
Mixed, high oxen +10% 1.4% 0.3% −16.8% 6.7% −4.5% −3.3% −0.6% 3.8%
Mixed, high oxen −10% −1.4% −0.3% 24.3% −6.7% 4.9% 4.1% 0.6% −3.7%
Ethiopia, low oxen +10% 1.5% 0.3% −16.8% 6.4% −4.5% −1.7% −1.5% 0.6%
Ethiopia, low oxen −10% −1.5% −0.3% 24.5% −6.4% 5.0% 2.0% 1.5% −0.6%
Ethiopia, medium oxen +10% 1.6% 0.3% −16.8% 6.4% −4.6% −3.1% −1.1% 2.0%
Ethiopia, medium oxen −10% −1.6% −0.3% 24.3% −6.4% 5.1% 3.7% 1.0% −2.0%
Ethiopia, high oxen +10% 1.8% 0.3% −16.6% 6.2% −4.6% −3.5% −1.0% 3.7%
Ethiopia, high oxen −10% −1.8% −0.3% 23.9% −6.2% 5.1% 4.3% 0.9% −3.6%

4. Discussion
While the results are consistent with the expectation that improving health is likely to lead to
reductions in EI, the validity of the results depends on the input assumptions and the method used to
perform the calculations. The approach developed in this study allows multiple effects of a disease
to be quantified. The MTB model enables herd growth and livestock movement over time to be
quantified. The use of a herd model in GLEAM enables disease impacts on parameters that affect
the herd structure to be modelled, e.g. death rates, fertility rates, replacement rates, and offtake
rates. The IPCC tier 2 approach [40] to calculating livestock emissions used in GLEAM enables
disease impacts on parameters that affect the production and emissions of the individual animal to

232
Sustainability 2018, 10, 1633

be modelled, e.g., milk yield, animal growth rates, activity level and ration. However, the approach
requires further development in order to capture some potentially important effects, such as the impact
of disease status on ration quality.
The results are expressed in terms of the functional unit “kg of CO2 e per kg of edible protein at
the farm gate”, and therefore don’t include post-farm emissions or take into account post-farm losses.
While post-farm emissions are likely to represent a small % of the total emissions, losses can make
significant differences to the EI, and may vary between different production systems. The functional
unit also assumes that: (a) 1 kg of milk protein is equivalent to 1 kg of meat protein and (b) production
of edible outputs is the only reason for keeping cattle, which are simplifications. Although some of
the emissions are allocated to draught power, none are allocated to other outputs (such as manure)
or the less tangible values that cattle may have, such as social value and increased resilience of their
owners [39]. While the choice of functional unit means that care needs to be taken when making
comparisons of the EI between systems, none of the limitations noted above would affect the change
in EI arising from treatment of trypanosomiasis.
As noted in [25] “data on livestock productivity (fertility, mortality, milk yields and output of
draught power) were mostly obtained from a limited number of in-depth studies in specific localities.
As the large number of references testifies, cattle systems in the study region have been much studied
and there is enough information to paint a good general picture, and to cross-check and validate.
However, although trypanosomosis has been relatively well researched, there remains a need for
more specific studies on this disease’s impact”. This is particularly the case with draught animals.
FAO have developed a geospatial database [70] that should improve understanding of trypanosomiasis
prevalence in Africa.

5. Conclusions
The treatment of trypanosomiasis in East African cattle systems could lead to reductions in EI
of between 0 and 8%, depending on the system. EI is closely related to productivity, and the largest
reductions in EI are in those systems experiencing the largest increases in productivity, i.e., the higher
(milk yield) dairy systems. However, when making inter-system comparisons, it should be borne in
mind that in some systems cattle perform functions in addition to producing meat and milk.
The approach employed in this study could, in principle, be used to model the impact of other
important diseases in SSA (such as foot and mouth disease), if their effects can be adequately described
in terms of the model parameters. However, in order to produce valid results, the main direct effects
of the disease need to be captured by the model. This is potentially challenging given the lack of data
on prevalence and impact for many diseases. While it may be possible to partially fill gaps through the
analysis of existing datasets (such as abattoir records), some diseases have important effects that are
not routinely recorded or readily measured (for example they may alter feed intake, the efficiency of
digestion or energy partitioning) and may require bespoke studies. A second challenge is capturing
the indirect effects of disease control. For example, disease treatment would lead to increased livestock
populations which could, depending on how this increase is managed, lead to overstocking and thus
reduced feed availability and/or quality.
The reduction of EI represents an external benefit of disease control, i.e., it is a benefit not normally
factored into farm management or policy decisions. In order to achieve the economically optimal
level of disease control, such externalities need to be quantified and included in decision making,
alongside other costs and benefits. Given the difficulty of measuring agricultural GHG emissions
directly, it is suggested that modelling approaches, such as the one outlined in this paper, have an
important contribution to make to the development of disease control strategies.

Author Contributions: Conceptualization, M.M. and T.R.; Data curation, M.M., W.W., and A.S.; Formal analysis,
M.M. and A.S.; Funding acquisition, T.R.; Investigation, V.E., W.W., A.S., P.G., G.C., and R.M.; Methodology, M.M.;
Writing—original draft, M.M.

233
Sustainability 2018, 10, 1633

Acknowledgments: This project was funded by the International Livestock Research Institute under CCAFS, the
CGIAR Research Program “Climate Change, Agriculture and Food Security”. The authors are grateful to the
UN FAO for permission to use GLEAM in this study. The authors would like to acknowledge the support of the
Scottish Government Strategic Research Programme, Theme 2: Productive and Sustainable Land Management
and Rural Economies. The support of the Government of Italy through the FAO Project “Improving food security
in sub-Saharan Africa by supporting the progressive reduction of tsetse-transmitted trypanosomiasis in the
framework of the NEPAD” (codes GTFS/RAF/474/ITA and GCP/RAF/502/ITA) is also acknowledged.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Robinson, T.P.; Pozzi, F. Mapping Supply and Demand for Animal-Source Foods to 2030; Animal Production and
Health Working Paper No. 2; Food and Agriculture Organisation of the United Nations: Rome, Italy, 2011.
2. Alexandratos, N.; Bruinsma, J. World Agriculture towards 2030/2050. The 2012 Revision. Global Perspective
Studies Team; ESA Working Paper No. 12-03; Food and Agriculture Organization of the United Nations:
Rome, Italy, 2012.
3. Pingali, P.; McCullough, E. Drivers of change in global agricultural livestock systems. In Livestock in
a Changing Landscape: Drivers, Consequences and Responses; Steineld, H., Mooney, H.A., Schneider, F.,
Neville, L.E., Eds.; Island Press: Washington, DC, USA, 2010.
4. Gerber, P.J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G.
Tackling Climate Change through Livestock—A Global Assessment of Emissions and Mitigation Opportunities;
Food and Agriculture Organization of the United Nations: Rome, Italy, 2013.
5. Vallat, B. Feeding the World Better by Controlling Animal Diseases. Available online: http://www.oie.
int/for-the-media/editorials/detail/article/feeding-the-world-better-by-controlling-animal-diseases/
(accessed on 23 May 2014).
6. Elliot, J. Animal health and productivity in the EU—Current and emerging issues. In Proceedings of the
FACCE–JPI Workshop: Animal Health/Animal Diseases and GHG Mitigation, Madrid, Spain, 21 May 2014.
7. MacLeod, M.; Eory, V.; Gruère, G.; Lankoski, J. Cost-Effectiveness of Greenhouse Gas Mitigation Measures for
Agriculture: A Literature Review, OECD Food; Agriculture and Fisheries Papers, No. 89; OECD Publishing:
Paris, France, 2015.
8. Stocker, T.F.; Qin, D.; Plattner, G.-K.; Tignor, M.; Allen, S.K.; Boschung, J.; Nauels, A.; Xia, Y.; Bex, V.;
Midgley, P.M. IPCC Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth
Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge,
UK; New York, NY, USA, 2013; p. 1535.
9. Hospido, A.; Sonesson, U. The environmental impact of mastitis: A case study of dairy herds.
Sci. Total Environ. 2005, 343, 71–82. [CrossRef] [PubMed]
10. Stott, A.; MacLeod, M.; Moran, D. Reducing Greenhouse Gas Emissions through Better Animal Health Rural Policy
Centre Policy Briefing July 2010 (RPC PB 2010/01); SAC: Edinburgh, UK, 2010.
11. Guelbenzu, M.; Graham, D. Prevalence of BVD in Northern Ireland Dairy and Suckler Herds; Agri-Food and
Biosciences Institute: Belfast, UK, 2013.
12. ADAS UK Ltd. Study to Model the Impact of Controlling Endemic Cattle Diseases and Conditions on National
Cattle Productivity; Agricultural Performance and Greenhouse Gas Emissions: Final Report; Defra/AVHLA:
London, UK, 2014.
13. Houdijk, J.G.M.; Tolkamp, B.J.; Rooke, J.A.; Hutchings, M.R. Animal health and greenhouse gas intensity:
The paradox of periparturient parasitism. Int. J. Parasitol. 2017, 47, 633–641. [CrossRef] [PubMed]
14. Opio, C.; Gerber, P.; Mottet, A.; Falcucci, A.; Tempio, G.; MacLeod, M.; Vellinga, T.; Henderson, B.; Steinfeld, H.
Greenhouse Gas Emissions from Ruminant Supply Chains—A Global Life Cycle Assessment; Food and Agriculture
Organization of the United Nations: Rome, Italy, 2013.
15. Staal, S.; Poole, J.; Baltenweck, I.; Mwacharo, J.; Notenbaert, A.; Randolph, T.; Thorpe, W.; Nzuma, J.;
Herrero, M. Targeting Strategic Investment in Livestock Development as a Vehicle for Rural Livelihoods. BMGF-ILRI
Project on Livestock Knowledge Generation; International Livestock Research Institute: Nairobi, Kenya, 2009.

234
Sustainability 2018, 10, 1633

16. Hristov, A.N.; Oh, J.; Lee, C.; Meinen, R.; Montes, F.; Ott, T.; Firkins, J.; Rotz, A.; Dell, C.; Adesogan, A.;
et al. Mitigation of Greenhouse Gas Emissions in Livestock Production—A Review of Technical Options for Non-CO2
Emissions; Gerber, P.J., Henderson, B., Makkar, H.P.S., Eds.; FAO Animal Production and Health Paper
No. 177; Food and Agriculture Organization of the United Nations: Rome, Italy, 2013.
17. Cecchi, G.; Mattioli, R.; Slingenbergh, J.; De La Rocque, S. Land cover and tsetse fly distributions in
sub-Saharan Africa. Med. Vet. Entomol 2008, 22, 364–373. [CrossRef] [PubMed]
18. Cattand, P.; Simarro, P.; Jannin, J.; Ly, C.; Fall, A.; Shaw, A.; Mattioli, R. Linking Sustainable Human and
Animal African Trypanosomiasis Control with Rural Development Strategies; Programme Against African
Trypanosomiasis–Technical and Scientific Series. Vol. 10. 2010; Food and Agriculture Organization of
the United Nations: Rome, Italy, 2010.
19. Simarro, P.P.; Cecchi, G.; Franco, J.R.; Paone, M.; Diarra, A.; Ruiz-Postigo, J.A.; Fèvre, E.M.; Mattioli, R.;
Jannin, J.G. Estimating and mapping the population at risk of sleeping sickness. PLoS Negl. Trop. Dis. 2012,
6, 1859. [CrossRef] [PubMed]
20. Taylor, K.; Authié, E.M.-L. Pathogenesis of Animal Trypanosomiasis. In The Trypanosomiases; Maudlin, I.,
Holmes, P.H., Miles, M.A., Eds.; CAB International: Wallingford, UK, 2004.
21. Diall, O.; Cecchi, G.; Wanda, G.; Argilés-Herrero, R.; Vreysen, M.J.B.; Cattoli, G.; Viljoen, G.J.; Mattioli, R.;
Bouyer, J. Developing a Progressive Control Pathway for African Animal Trypanosomosis. Trends Parasitol.
2017, 33, 499–509. [CrossRef] [PubMed]
22. IGAD. The IGAD Region. Available online: https://igad.int/index.php/about-us/the-igad-region (accessed
on 24 September 2017).
23. FAOSTAT Live Animals. Available online: http://www.fao.org/faostat/en/#data/QA (accessed on 9 May 2018).
24. Cecchi, G.; Wint, W.; Shaw, A.; Marletta, A.; Mattioli, R.; Robinson, T. Geographic distribution and
environmental characterization of livestock production systems in Eastern Africa. Agric. Ecosyst. Environ.
2010, 135, 98–110. [CrossRef]
25. Shaw, A.P.M.; Cecchi, G.; Wint, G.R.W.; Mattioli, R.C.; Robinson, T.P. Mapping the economic benefits of
intervening against bovine trypanosomiasis in Eastern Africa. Prev. Vet. Med. 2014, 113, 197–210. [CrossRef]
[PubMed]
26. Mwai, O.; Hanotte, O.; Kwon, Y.-J.; Cho, S. African Indigenous Cattle: Unique Genetic Resources in a Rapidly
Changing World. Asian-Australas. J. Anim. Sci. 2015, 28, 911–921. [CrossRef] [PubMed]
27. Domestic Animal Genetic Resources Information System (DAGRIS). Available online: http://dagris.info/
(accessed on 9 May 2018).
28. Shaw, A.; Wint, W.; Cecchi, G.; Torr, S.; Waiswa, C.; Alemu, T.; Eregae, M.; Abdi, A.; Muchina, S.; Mugasi, S.;
et al. Intervening against Bovine Trypanosomosis in Eastern Africa: Mapping the Costs and Benefits; PAAT Technical
and Scientific Series No. 11; FAO: Rome, Italy, 2017; Available online: http://www.fao.org/3/a-i7342e.pdf
(accessed on 15 May 2018).
29. Itty, P. Economics of Village Cattle Production in Tsetse-affected Areas of Africa. In A Study of Trypanosomiasis
Control Using Trypanotolerant Cattle and Chemotherapy in Ethiopia, Kenya, The Gambia, Côte d’Ivoire, Zaire and
Togo; Hartung-Gorre Verlag: Constance, Germany, 1992.
30. Starkey, P.; Kaumbutho, P. Meeting the Challenges of Animal Traction. In A Resource Book of the Animal
Traction Network for East-ern and Southern Africa (ATNESA), Harare, Zimbabwe; Intermediate Technology
Publications: London, UK, 1999.
31. Rege, J.E.O.; Kahi, A.K.; Okomo-Adhiambo, M.; Mwacharo, J.; Hanotte, O. Zebu Cattle of Kenya: Uses,
Performance, Farmer Preferences, Measures of Genetic Diversity; ILRI (International Livestock Research Institute)
and Kenya Agriculture Research Institute (KARI): Nairobi, Kenya, 2001.
32. Otte, M.J.; Chilonda, P. Cattle and Small Ruminant Production Systems in Sub-Saharan Africa. A Systematic
Review; FAO (Food and Agriculture Organization of the United Nations): Rome, Italy, 2002.
33. Ocaido, M.; Otim, C.; Okuna, N.; Erume, J.; Ssekitto, C.; Wafula, R.; Kakaire, D.; Walubengo, J.; Monrad, J.
Socio-economic and livestock disease survey of agro-pastoral communities in Serere County, Soroti District,
Uganda. Livest. Res. Rural Dev. 2005, 17, 93.
34. Shaw, A.P.M.; Wint, G.R.W.; Cecchi, G.; Torr, S.J.; Mattioli, R.C.; Robinson, T.P. Mapping the benefit-cost
ratios of interventions against bovine trypanosomiasis in Eastern Africa. Prev. Vet. Med. 2015, 122, 406–416.
[CrossRef] [PubMed]

235
Sustainability 2018, 10, 1633

35. MacLeod, M.J.; Vellinga, T.; Opio, C.; Falcucci, A.; Tempio, G.; Henderson, B.; Makkar, H.; Mottet, A.;
Robinson, T.; Steinfeld, H.; et al. Invited Review: A Position on the Global Livestock Environmental
Assessment Model (GLEAM). Animal 2018, 12, 383–397. [CrossRef] [PubMed]
36. Wint, G.R.W. Kilometre Resolution Tsetse Fly Distribution Maps for the Lake Victoria Basin and West Africa; Report
to the Joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency
Programme; Food and Agriculture Organization: Rome, Italy, 2001.
37. Wint, W.; Rogers, D. Predicted Distributions of Tsetse in Africa; Report of the Environmental Research Group
Oxford Ltd and TALA Research Group, Department of Zoology, University of Oxford, for the Animal Health
Service of the Animal Production and Health Division of the Food and Agriculture Organisation of the
United Nations; FAO: Rome, Italy, 2000.
38. Wint, W.; Robinson, T. Gridded Livestock of the World; FAO (Food and Agricultural Organization of the United
Nations): Rome, Italy, 2007.
39. Weiler, V.; Udo, H.M.; Viets, T.; Crane, T.A.; De Boer, I.J. Handling multi-functionality of livestock in a life
cycle assessment: The case of smallholder dairying in Kenya. Curr. Opin. Environ. Sustain. 2014, 8, 29–38.
[CrossRef]
40. IPCC. IPCC Guidelines for National Greenhouse Gas Inventories; Prepared by the National Greenhouse Gas
Inventories Programme; Eggleston, H.S., Buendia, L., Miwa, K., Ngara, T., Tanabe, K., Eds.; IPCC: Kanagawa,
Japan, 2006.
41. Peeler, E.; Omore, A. Manual of Livestock Production Systems in Kenya; KARI (Kenya Agricultural Research
Institute): Nairobi, Kenya, 1997.
42. Roderick, S.; Stevenson, P.; Mwendia, C.; Okech, G. The use of trypanocides and antibiotics by Maasai
pastoralists. Trop. Anim. Health Prod. 2000, 32, 361–374. [CrossRef] [PubMed]
43. Roderick, S.; Stevenson, P.; Ndungu, J. The production parameters influencing the composition and structure
of pastoral cattle herds in a semi-arid area of Kenya. Anim. Sci. 1998, 66, 585–594. [CrossRef]
44. Roderick, S.; Stevenson, P.; Ndungu, J. Factors influencing the production of milk from pastoral cattle herds
in Kenya. Anim. Sci. 1999, 68, 201–209.
45. Itty, P.; Swallow, B.; Rowlands, G.; Mulatu, W.; d’Ieteren, G. The economics of village cattle production in a
tsetse-infested area of southwest Ethiopia. Prev. Vet. Med. 1995, 22, 183–196. [CrossRef]
46. Swallow, B. Impacts of Trypanosomiasis on African Agriculture; Food and Agriculture Organization of the
United Nations (FAO): Rome, Italy, 2000.
47. Muraguri, G.R. Epidemiological and Financial Impact of Vector-borne Diseases on Productivity of Smallholder Cattle
in the Coastal Lowlands of Kenya; Department of Agriculture, University of Reading: Reading, UK, 2000; p. 219.
48. Machila, N. Improved Targeting and Appropriate Use of Trypanocidal Drugs for the Control of African Bovine
Trypanosomiasis in Tsetse Endemic Areas of Western and Coastal Kenya within the Context of Primary Veterinary
Care; University of Edinburgh: Edinburgh, UK, 2005; p. 304.
49. Musa, L.; Peters, K.; Ahmed, M. On farm characterization of Butana and Kenana cattle breed production
systems in Sudan. Livest. Res. Rural Dev. 2006, 18, 177.
50. Maichomo, M.; Ndungu, J.; Ngare, P.; Ole-Mapenay, I. The performance of Orma Boran and Maasai Zebu
crossbreeds in a trypanosomiasis endemic area of Nguruman, south western Kenya. Onderstepoort J. Vet. Res.
2010, 72, 87–93.
51. Omore, A.; Muriuki, H.; Kenyanjui, M.; Owango, M.; Staal, S. The Kenyan Dairy Sub-Sector: A Rapid Appraisal;
Smallholder Dairy (Research & Development) Project Report; ILRI (International Live-stock Research
Institute): Nairobi, Kenya, 1999.
52. Mudavadi, P.O.; Otieno, K.J.; Wanambacha, W.; Odenya, J.O.; Odendo, M.; Njaro, O.K. Smallholder Dairy
Production and Marketing in Western Kenya: A Review of Literature; Smallholder Dairy (Research & Development)
Project Research Report; ILRI (International Livestock Research Institute): Nairobi, Kenya, 2001.
53. Ongadi, P.; Wakhungu, J.; Wahome, R.; Okitoi, L. Characterization of grade dairy cattle owning households
in mixed small scale farming systems of Vihiga, Kenya. Livest. Res. Rural Dev. 2007, 19, 43.
54. Fox, R.G.R.; Mmbando, S.; Fox, M.; Wilson, A. Effect on herd health and productivity of controlling tsetse and
trypanosomiasis by applying deltamethrin to cattle. Trop. Anim. Health Prod. 1993, 25, 203–214. [CrossRef]
[PubMed]
55. Jemal, A.; Hugh-Jones, M.E. Association of tsetse control with health and productivity of cattle in the Didessa
Valley, western Ethiopia. Prev. Vet. Med. 1995, 22, 29–40. [CrossRef]

236
Sustainability 2018, 10, 1633

56. Laker, C.D. Assessment of the Economic Impact of Bovine Trypanosomiasis and its Control in Dairy Cattle in Mukono
County, Uganda; Makerere University: Kampala, Uganda, 1998.
57. Rowlands, G.; Mulatu, W.; Leak, S.; Nagda, S.; d’Ieteren, G. Estimating the effects of tsetse control on
livestock productivity—A case study in southwest Ethiopia. Trop. Anim. Health Prod. 1999, 31, 279–294.
[CrossRef] [PubMed]
58. Shaw, A. Economics of African trypanosomiasis. In The Trypanosomiases; Maudlin, I., Holmes, P., Miles, M., Eds.;
CABI Publishing: Wallingford, UK, 2004; pp. 369–402.
59. Mugunieri, G.; Matete, G. Association of trypanosomiasis risk with dairy cattle production in western Kenya.
Onderstepoort J. Vet. Res. 2005, 72, 279–284. [CrossRef] [PubMed]
60. Minjauw, B.; McLeod, A. Tick-borne Diseases and Poverty; DFID Animal Health Programme: Edinburgh,
UK, 2003.
61. Tesfaye, D.; Speybroeck, N.; De Deken, R.; Thys, E. Economic burden of bovine trypanosomiasis in three
villages of Metekel zone, Northwest Ethiopia. Trop. Anim. Health Prod. 2012, 44, 873–879. [CrossRef]
[PubMed]
62. Wilson, R.T.; Bech, J.N.; Waveren, E. Draught animals in the livelihoods of mixed smallholder farmers in
North Wollo, Ethiopia. Draught Anim. News 2002, 37, 2–8.
63. You, L.; Guo, Z.; Koo, J.; Sebastian, K.; Wood-Sichra, U. Spatial Production Allocation Model (SPAM) 2005
Version 1; Provided through Harvest Choice; International Food Policy Research Institute: Washington,
DC, USA; University of Minnesota: St. Paul, MN, USA, 2014; Available online: http://harvestchoice.org
(accessed on 8 January 2015).
64. Lukuyu, B.; Gachuiri, C.K.; Lukuyu, M.N.; Lusweti, C.; Mwendia, S. Feeding Dairy Cattle in East Africa; East
Africa Dairy Development Project: Nairobi, Kenya, 2012.
65. CGIAR/ILRI Sub-Saharan Africa Feed Composition Database. Available online: http://192.156.137.110/
ssafeed/ (accessed on 1 December 2015).
66. Feedipedia. Feedipedia Animal Feed Resources Information System, a Programme by INRA, CIRAD, AFZ
and FAO. Available online: http://www.feedipedia.org (accessed on 1 August 2015).
67. Feedipedia Napier Grass. Available online: https://www.feedipedia.org/node/395 (accessed on
13 December 2017).
68. Capper, J.L.; Cady, R.A.; Bauman, D.E. The environmental impact of dairy production: 1944 compared with
2007. J. Anim. Sci. 2009, 87, 2160–2167. [CrossRef] [PubMed]
69. Gerber, P.; Vellinga, T.; Opio, C.; Steinfeld, H. Productivity gains and greenhouse gas EI in dairy systems.
Livest. Sci. 2011, 139, 100–108. [CrossRef]
70. Cecchi, G.; Paone, M.; Feldmann, U.; Vreysen, M.J.B.; Diall, O.; Mattioli, R.C. Assembling a geospatial
database of tsetse-transmitted animal trypanosomiasis for Africa. Parasites Vectors 2014, 7, 39. [CrossRef]
[PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

237
 sustainability

Review
Reservoirs and Transmission Pathways of Resistant
Indicator Bacteria in the Biotope Pig Stable and
along the Food Chain: A Review from a One
Health Perspective
Ricarda Maria Schmithausen 1,* , Sophia Veronika Schulze-Geisthoevel 2, Céline Heinemann 2 ,
Gabriele Bierbaum 3, Martin Exner 1, Brigitte Petersen 2 and Julia Steinhoff-Wagner 2
1 Institute for Hygiene and Public Health, University Hospital Bonn, 53127 Bonn, Germany;
[email protected]
2 Institute of Animal Science, Preventive Health Management Group, University of Bonn, Katzenburgweg 7-9,
53115 Bonn, Germany; [email protected] (S.V.S.-G.);
[email protected] (C.H.); [email protected] (B.P.); [email protected] (J.S.-W.)
3 Institute for Medical Microbiology, Immunology and Parasitology, University Hospital of Bonn,
53127 Bonn, Germany; [email protected]
* Correspondence: [email protected]; Tel.: +49-228-287-13452

Received: 1 September 2018; Accepted: 22 October 2018; Published: 31 October 2018

Abstract: The holistic approach of “One Health” includes the consideration of possible links between
animals, humans, and the environment. In this review, an effort was made to highlight knowledge
gaps and various factors that contribute to the transmission of antibiotic-resistant bacteria between
these three reservoirs. Due to the broad scope of this topic, we focused on pig production and selected
“indicator bacteria”. In this context, the role of the bacteria livestock-associated methicillin-resistant
Staphylococcus aureus (LA-MRSA) and extended spectrum beta-lactamases carrying Escherichia coli
(ESBL-E) along the pig production was particularly addressed. Hotspots of their prevalence and
transmission are, for example, pig stable air for MRSA, or wastewater and manure for ESBL-E,
or even humans as vectors in close contact to pigs (farmers and veterinarians). Thus, this review
focuses on the biotope “stable environment” where humans and animals are both affected, but
also where the end of the food chain is not neglected. We provide basic background information
about antibiotics in livestock, MRSA, and ESBL-bacteria. We further present studies (predominantly
European studies) in tabular form regarding the risk potentials for the transmission of resistant
bacteria for humans, animals, and meat differentiated according to biotopes. However, we cannot
guarantee completeness as this was only intended to give a broad superficial overview. We point
out sustainable biotope approaches to try to contribute to policy management as critical assessment
points in pig housing conditions, environmental care, animal health, and food product safety and
quality as well as consumer acceptance have already been defined.

Keywords: MRSA; ESBL-E; pigs; transmission; antibiotic resistance; one health

1. Introduction
The use of antibiotics in human and veterinary medicine and their dissemination in the
environment have favored the emergence and spread of antibiotic-resistant microorganisms [1–5].
For example, both extended-spectrum betalactamase-producing Escherichia coli (ESBL-E) [6,7]
and livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) have already been
separately isolated at different stages of the pork production chain [8–11]. Hence, there has been
an ongoing debate regarding the potential sources, transmission routes, and risk factors of the

Sustainability 2018, 10, 3967; doi:10.3390/su10113967 238 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3967

continuous spread of MRSA and ESBL-E between animals, humans, and the environment [12–16].
Thus, they are also perceived as a potential threat to public health [17–23]. Therefore, in this review,
methicillin-resistant Staphylococcus aureus (MRSA) and ESBL-E have been used as “indicator” bacteria
with possible zoonotic potential and occurrence in both the stable biotopes and healthcare sector
and community [24]. Consequently, farmers have been confronted with several consequences of this
problem: The potential danger of animal colonization with drug-resistant bacteria for (i) humans living
on or in the vicinity of farms [25–27], and (ii) for consumers of animal products [3,28–31]. The intended
audience of this review is farmers of intensive pig production systems worldwide as well as healthcare
workers, as humans living and working in close contact with pigs and patients in rural areas have
been found to be colonized with LA-MRSA [25,32–38]. On the other hand, in the food chain, meat
products can serve as potential transmission factors of ESBL-E from animals to humans [29,39–41].
Furthermore, the global spread of multidrug-resistant Enterobacteriaceae may be linked to
wastewater from hotspots like hospitals and/or intensive livestock production settings in Germany and
worldwide [15,16]. Consequently, the stable environment (air, wastewater, etc.) needs to be considered
as a reservoir and source of the dissemination of multidrug-resistant bacteria. Notably, bacteria not only
persists on/in the living animal, but also on surfaces that are in contact with the animals (compartment
walls and equipment) [42]. In correlation with this, LA-MRSA bacteria were detected by Friese et al. [43]
in dust samples from the investigated breeding farms in Germany and in the stable air of a fattening
farm, while ESBL-Escherichia coli isolates have been isolated from pig livestock production sites [44].
Furthermore, in the farm environment, both commensal and environmental bacteria serve as reservoirs
for the transfer of antimicrobial resistance genes to pathogenic bacteria [45,46]. Pietsch et al. [47] found
isolates of distinct E. coli clonal lineages in all three reservoirs: Human, animal, and food in Germany.
Thus, it is assumed that the contribution of the animal biotope in terms of antimicrobial resistance in
humans is not negligible [48].
Therefore, a holistic approach in the sense of “One Health” needs to be integrated into
interdisciplinary research at the interface between humans and animals and their common
environment [49–52]. In the framework of sustainable biotope infection control measures in pig
housing conditions, hygienic stable environment, animal health, and food product safety to reduce the
prevalence of resistant bacteria remains challenging in pig production [53].

2. Background Information

2.1. Antibiotic Use in Livestock Production

The first cases of antimicrobial resistance occurred in the late 1930’s [54]. From that point until
now, the production of food animals has been associated with large farms, a high density of animals,
and in this respect, an improvement in disease management [2].
In a report on antibiotic consumption and resistance in Germany in 2015 (GERMAP), tetracycline,
sulfonamide, and betalactam antibiotics (penicillin, first to fourth generation cephalosporin, and the
betalactamase inhibitors) [55] were found to be the most commonly used antibiotics in veterinary
medicine [56]. The total consumption of around 1706 tons of antibiotics used in the veterinary field
in 2011 decreased to 733 tons in 2017 [57,58]. It can be assumed that the reduction was not only
based on the EU ban, but on the basis of governmental and private antibiotic monitoring programs.
However, the causal relationship between the decrease in resistance rates and the decrease in antibiotic
use, observed on behalf of the patient on the basis of the quantities administered and/or the frequency
of treatment, cannot be examined on the basis of the available data. Metaphylactic therapy (in
which high doses of antibiotics are usually given for a short period) is still preferred in the standard
management of some highly organized and efficient management systems due to the optimized disease
prevention rates [59,60]. The adaptation of bacterial metabolism to antimicrobial agents can be forced
by under-dosing and the non-achievement of required blood and tissue levels over several days.
To avoid the selection of drug-resistant bacteria, it is necessary to relate the dosage of antibiotics to

239
Sustainability 2018, 10, 3967

body mass and perform several repeat applications [61]. Further data has shown a correlation between
the frequency of treatment and the occurrence of multidrug-resistant bacteria. The higher the treatment
frequency (the average number of days each animal in the herd is treated with antibiotics), the higher
the rate of resistance identified in isolates from animals and animal products [62,63]. Fundamentally,
animal protection laws demand that animals with infections have the right to (medical) treatment [64].
Furthermore, the use of antibiotics is indicated for the maintenance of a balanced pig’s health and its
physical condition [65,66].

2.2. Characteristics of Multidrug-Resistant Bacteria (MRSA and ESBL-E)

2.2.1. MRSA
S. aureus is a Gram-positive, coagulase-positive bacterium. S. aureus demonstrates a high
robustness of months for desiccation, heat, UV radiation, and various disinfectants [67]. S. aureus
can transiently or persistently colonize the skin and mucous membranes of the respiratory tract
of humans and animals [68]. Colonization alone does not cause symptoms, but can lead to an
increased risk for secondary infections: superficial skin lesions and soft tissue infections, invasive
life-threatening bloodstream infections, and sepsis [67]. Methicillin-resistant Staphylococcus aureus
(MRSA) strains acquire their resistance by transferring the mobile genetic element, SCCmec [69].
The resistance is based on the mecA gene on the SCCmec coding for the 78 kDa alternative penicillin
binding protein (PBP2a) [70]. The PBP2a has a very low binding affinity for all betalactam
antibiotics. This allows the PBP2a to synthesize the cross-links of the peptidoglycan of the bacterial
cell wall without being inhibited by methicillin and any traditional beta-lactam antibiotics [71].
However, new “5th generation” cephalosporins (ceftaroline and ceftobiprole) have a high affinity
for this PBP, resulting in enhanced activity against methicillin-resistant S. aureus [72–74]. MRSA
in humans was first isolated in the United Kingdom and Denmark after penicillinase-stable
betalactam methicillin was introduced in 1959 [75,76]. In animals, MRSA was identified in 1972 [77].
Three different MRSA types linked with human infection can be classified based on their occurrence
and distribution patterns: hospital-associated MRSA (HA-MRSA), health care-associated community
MRSA (HCA-MRSA), and community-associated MRSA (CA-MRSA) [78,79]. The fourth category is
called livestock-associated MRSA (LA-MRSA) and is associated with livestock as well as the humans
who are in close contact with the livestock [78]. LA-MRSA has retained a pathogenic potency for
humans [80,81] although some virulence factors have been lost [78]. This underlines the potential of
“bidirectional zoonotic exchange”, which adds risks to public health [78]. Most LA-MRSA strains are
classified as clonal lineage CC398 [79,82]. Price et al. [78] assumed that clonal lineages of LA-MRSA
CC398 originated from human methicillin-sensitive Staphylococcus aureus (MSSA), which has adapted
to livestock animals [78,83].

2.2.2. ESBL and Resistance Genes

Extended-spectrum betalactamases (ESBLs) and the less common AmpC enzyme are able
to hydrolyze a broader spectrum of betalactam antibiotics than the original betalactamases from
which they are derived. ESBLs inactivate betalactam antibiotics with an oxyimino group such
as oxyimino-cephalosporin (e.g., ceftazidime and cefotaxime) and the oxyimino-monobactam
aztreonam [84,85]. ESBL and AmpC enzymes can combine to expand the resistance profile to
include betalactamase inhibitors and even carbapenems [86]. Paterson et al. [87] also described
ciprofloxacin resistance as being highly associated with ESBL-producing strains [87]. A further
increase in resistance is provided by carbapenemases (e.g., VIM [Verona integron-encoded
metallo-betalactamase], NDM [New Delhi metallo-betalactamase], OXA-48 [oxacillin resistant]) [88],
which are betalactamases that are able to hydrolyze the carbapenem reserve antibiotics (imipenem,
meropenem, and ertapenem) [89,90]. The most common types of ESBL enzymes detected in
Enterobacteriaceae are the following: Temoneira (TEM)-type betalactamase, cefotaximase-Munich

240
Sustainability 2018, 10, 3967

(CTX-M)-type betalactamase, sulfhydryl variable (SHV)-type betalactamase, and oxacillin resistant

(OXA)-type betalactamase [91]. Currently, the most common worldwide CTX-M-type enzymes can
be classified into five main groups depending on their amino acid sequence: CTX-M-1, CTX-M-2,
CTX-M-8, CTX-M-9, and CTX-M-25 [13,92–94]. There are more than 40 different CTX-M types
assigned to the five main groups [95]. The enzyme that is most widely distributed between
human Enterobacteriaceae is CTX-M-15, which has also been detected in E. coli from pigs and
poultry [96,97]. The genes for ESBL (blaCTX-M genes) [98,99] are transferred by both vertical and
horizontal transfer [100]. Therefore, apart from direct transmission in Enterobacteriaceae, it is of
particular interest that resistance genes can be transferred with the help of plasmids to other pathogenic
and apathogenic microorganisms. They encode a variety of resistance genes [101]. MGEs appear in a
huge variety: Transposons, phages, plasmids, chromosomal resistance cassettes, and others, which can
be taken up by bacteria in different biotopes [102]. However, the role of antibiotic resistance genes
and their exchange of resistance genes between the human and animal microflora and between the
environment is not completely known [103].

2.3. Bioavailability and Transmission Potential of Antibiotic-Resistant Bacteria

The following aspects can be discussed to influence the spread and bioavailability of drug-resistant
bacteria in different reservoirs in Table S1 in the Supplementary Material.

3. Reservoirs and Transmission Pathways of LA-MRSA and ESBL-E

3.1. Transmission Pathways

The epidemiology and mechanisms of emergence and spread of antimicrobial resistance and
antibiotic-resistant bacteria are diverse and several possible pathways in different systems exist for
their transmission. Valentin et al. [104] indicated that the same subtypes of isolates were detected
in isolates from human and livestock and companion animal populations, suggesting a possible
exchange of bacteria or bacterial genes. Figure 1 presents some possible transmission pathways of
antibiotic-resistant bacteria between human and animal vectors and between reservoirs (air, dust, water,
manure, food, etc.) as well as exposure routes in their biotopes (stable, abattoir, etc.). Here, the term
“biotope” is defined according to Nehring and Albrecht [105] and Lötzli [106] as the living space of a
community of species.
Nevertheless, many transmission routes are still unclear. Therefore, in the following passages,
a selection of possible transmission pathways in different biotopes and reservoirs will be demonstrated
using the selected bacteria MRSA and ESBL-E. We used both MRSA and ESBL-producing E. coli
(ESBL-E) as indicators to evaluate the movement of antibiotic-resistant bacteria in the environment [24]
as Staphylococcus aureus occurs in both the mucous membrane of humans and animals and is
very resistant to the environment. The MRSA strain CC398 is known to be transferred via direct
contact between animals [107] and humans [25,108–110], as well as through the environment [111],
particularly airborne transmission [43,112]. On the other hand, Escherichia coli is frequently used
as indicator bacteria in the animal sector and in environmental hygiene. Additionally, due to its
association with swine and pork, we decided to use the resistant variant ESBL-E [113,114]. In the
following sections, the different sources and reservoirs, especially within the stable environment,
are presented and discussed in more detail regarding the different transmission potentials.

241
Sustainability 2018, 10, 3967





 
 
















 






 



 

   

       

  




     
    




Figure 1. Some possible routes of exposure and transmission pathways of antibiotic-resistant bacteria
and antimicrobial resistance between different reservoirs and biotopes.

3.2. LA-MRSA and ESBL-E in Humans in the Stable Biotope

The administration of antibiotics in humans and animals selects resistant strains within the
microflora and enables colonization of the mucosa with new isolates. Animal strains may be able to
transiently colonize human indigenous microflora (and vice versa) and transfer resistance genes [115].
Thus, the human respiratory and gastrointestinal tract can be reservoirs for bacteria with antibiotic
resistance [116] (Table S2). Humans working in the stable environment make contact with different
resistant strains which can act as vectors in different biotopes [117]: Farmers and veterinarians
belong to the stable’s biotope [118]. Pig farmers and veterinarians belong to this defined risk
group [119]. Table S2 gives an overview over the occurrence of MRSA and ESBL-E rates in farmers
and veterinarians in Europe and possible transmission pathways. Nevertheless, the importance of
drug-resistant Staphylococcus aureus and/or E. coli strains isolated from the animal biotope has not yet
been quantified or evaluated. However, it is assumed that the contribution of the animal biotope in
terms of antimicrobial resistance in humans is not negligible [48]. Kraemer et al. [120] even showed
associations between antibiotic use and resistant bacteria carriage.

3.3. LA-MRSA and ESBL-E in Pigs

Possible sources for the transmission of drug-resistant bacteria and/or antimicrobial resistances
include direct contact between animals on the farm and within compartments [121,122] or via pig
trading [9,10] in livestock vehicles [123] within or between regions, and the introduction of new
animals in herds [124,125]. Pigs can also be colonized during transportation between pig production
steps or on their way to the abattoir [8,126]. Until now, the LA-MRSA CC398 strain has been found
in all stages of the food chain, varying between European countries (Table S3). Other risk factors are
reported to be associated with the occurrence of multidrug-resistant bacteria are for antimicrobial use,
purchase of gilts, and hygiene measures [127,128]. Generally, the effectiveness of the cleaning and
disinfection methods used on commercial pig farms needs to be evaluated in more detail [129,130].
Table S3 gives an overview of several studies describing the different possibilities of the
transmission of antibiotic-resistant bacteria (MRSA and ESBL-E) between pigs.

242
Sustainability 2018, 10, 3967

3.4. Reservoir Stable Environment

Studies on the agricultural environment and the food chain have revealed that pathogen
reservoirs also exist in the environment outside their animal host [129,131–134]. In farm environments,
commensal, and environmental bacteria may be reservoirs for the transfer of antimicrobial resistance
genes to pathogenic bacteria [97,135–138].

3.4.1. LA-MRSA and ESBL-E in Air and Dust

Dynamic processes influencing the spread of bacteria in the biotope of the animal stable are
presented in Figure 2.

Figure 2. Dynamic processes of bacteria in the biotope of the animal stable (modified according to
Müller et al. [139]). Bacteria can spread from their source via different dynamic processes:

• Turbulence: Spread of bacteria due to air turbulence;

• Mechanical contact: Transmission of bacteria by direct contact (passive via stable equipment or
active via persons/animals);
• Sedimentation: Reduction of circulation from the airborne state and subsequent deposit;
• Re-suspension: Bacteria not primarily and actively transported by air flow; and
• Re-entrainment: Re-return of already sedimented bacteria to the air [139].

In the pig stable, about 80% of airborne bacteria are staphylococci (Gram positive) [140] and
0.5% [141] or even 5% [142] are coliform bacteria such as E. coli (Gram negative). The imbalance between
Gram-positive and Gram-negative bacteria is attributed to the lower survival time of Gram-negative
bacteria in their airborne condition [141]. S. aureus can disperse in the air as directly suspendable
airborne particles. However, they are most often attached to and carried by dust particles [141].
Once the microorganisms get into the air, they prefer to merge into larger clusters or adhere to larger
dust particles. Airborne bacteria return via air turbulence or by sedimentation to their reservoirs on
stable surfaces or are acquired by animals or humans [126,128,143]. In contrast, coliform bacteria,

243
Sustainability 2018, 10, 3967

which are excreted in feces, are mechanically bound to stable surfaces and/or litter and feed [144].
Only after the animal feces have dried out, and due to air turbulence by animal activities, does the
whirling dust and dirt particles raise them in the stable air. The level of contamination of stable air by
both airborne and coliform bacteria depends on both the animal and stable environment including the
density, age, and activity of animals, the ventilation system, the quantity of dust [145], the humidity
of the surfaces, and air as well as air turbulence. Survival of intestinal bacteria depends on the
environmental conditions outside the animal organism. Survival rates of coliforms are best in the
immediate vicinity of the animal and, therefore, in feces and fecal contaminated surfaces, whereas the
detection rate in air immediately decreases [146–148]. The bacterial concentration in the air is based
on physical processes (e.g., air flow and sedimentation) and on the organisms’ biological viability.
Influencing factors are temperature, humidity, UV radiation, air change rate, noxious gas concentration,
and the organisms’ aerodynamic shape [63,149].
Environmental contamination with MRSA was identified in the study by Weese et al. [150].
Friese et al. [43] determined that 85.2% of pig stables in Germany were LA-MRSA positive in the air.
They also identified dust as an important factor for the occurrence of MRSA in the air. Drug-resistant
S. aureus could be identified inside and outside the pig stables and originated from contaminated
dust [151]. The dissemination of MRSA between pigs within a farm by air was based on a positive
association of samples from pigs and the environment [43]. Agersø et al. [112] indicated a high
sensitivity of air samples equal to the within-herd prevalence. Therefore, they recommended air
sampling for initial testing or even screening of herds. Bos et al. [152] and Gilbert et al. [111] even
confirmed a strong association between nasal ST398 MRSA carriage in people working on the farms
for >20 h per week and MRSA air levels. In people working in the barns <20 h per week, there was
a strong association between nasal carriage and the number of working hours. This study showed
that working in the lairage area or scalding and dehairing area were the major risk factors for MRSA
carriage in pig slaughterhouse workers, while the overall prevalence of MRSA carriage was low.
Occupational exposure to MRSA decreased along the slaughter line, and the risk of carriage showed a
parallel decrease. Heinemann et al. [153] showed that a working time of three-to-six hours could be
enough for positive findings of nasal colonization with MRSA. However, it is unknown whether the
presence of LA-MRSA is a result of the carriage or retention of MRSA-contaminated dust. Nevertheless,
the persistence of LA-MRSA CC398 in humans depends on the intensity of animal contact [109]. Several
studies have investigated dust and air samples from pig farms. An overview of some of these studies
and their data is given in Table S4.
The main message of all the presented studies (in Table S4) is that exposure to the stable
environment and air in pig farms is often contaminated with LA-MRSA, and can act as a transmission
source for humans, which is an important determinant for nasal carriage, especially in this highly
exposed group of farmers. This is next to the duration of the contact with animals. Intervention
measures should therefore also target the reduction of ST398 MRSA air levels including the
improvement of environmental and operating parameters of air quality and pig performance [154,155].
In contrast, only a few studies have been performed on the spread of ESBL-E in the stable environment
such as by dust and air in pig settings [126,156–158]. Laube et al. [159] assumed dust to be a major
source for the transmission and spread of ESBL-E within stables and during the release of animals
(especially poultry) from stables. They found a high prevalence of ESBL-E in the pooled feces and dust
samples obtained on broiler chicken farms [159]. Von Salviati et al. [157] identified the transmission
potential between ESBL-E between pig farmers and their surroundings (surfaces, barn, and ambient air).
However, the detection of ESBL/AmpC–E. coli in stable air and ambient environment was low and also
found ESBL/AmpC–E. coli on surfaces in the vicinity (see details in Table S4). Furthermore, they proved
emission via slurry and transmission via flies. Hoffmann [160] hypothesized a possible transmission
of CTX-M-1 subtypes to humans via the inhalation of contaminated dust particles during exposure
in the stable environment. This assumption was confirmed by the study of Dohmen et al. [158],

244
Sustainability 2018, 10, 3967

who found that CTX-M-1 carriage in pig farmers and the presence of CTX-M-1 in dust were associated,
indicating that air transmission of CTX-M 1 might be possible on pig farms.
In summary, the transmission pathway of ESBL-Enterobacteriaceae via air and/or dust spread
via the airborne route or via different vectors seems possible [127]. Otherwise, it is not possible to
distinguish between the two transmission pathways of direct contact between humans and animals
and the indirect airborne transmission pathway [160]. Contaminated manure presented the major
emission source for ESBL/AmpC-producing E. coli on pig farms [157].

3.4.2. LA-MRSA and ESBL-E in Water, Wastewater and Manure

Water contaminated with antibiotic-resistant bacteria is an important reservoir for the emergence
and spread of resistance mechanisms and mobile genetic elements [161,162]. Ingestion and dealing
with contaminated water can result in the colonization of the gastrointestinal tract of humans and
animals [163]. Thus, water constitutes not only a way for the dissemination of antibiotic-resistant
organisms among human and animal populations as drinking water is produced from surface water,
but also a major route by which resistance genes are introduced to natural bacterial ecosystems. In such
systems, nonpathogenic bacteria can serve as a reservoir of resistance genes [162]. Lupo et al. [161]
and Schwartz et al. [164] highlighted horizontal gene transfer by transduction as the main mechanism
conferring drug resistance in drinking water, surface water, and wastewater. Several other studies have
reported the presence of drug-resistant bacteria and resistance genes in fresh drinking water, rivers,
and sewage in Europe and all over the world [16,44,165–171]. Nevertheless, to date, more and more
information about the risks of contamination of livestock drinking water with antibiotic-resistant
bacteria have been provided [128,172,173]. Pletinckx et al. [174] did not find any evidence of
MRSA-positive isolates in animal drinking water on pig and poultry farms, while environmental
samples (dust, animal feed, and manure) and samples from pigs and farmers were contaminated
with MRSA. However, MRSA has been found in contaminated feed and trough water [130,172].
Thus, water sources might facilitate the transmission of MRSA between different animals [175].
Feed and troughs also represent possible sources of exposure to foodborne coliform bacteria like
E. coli [176]. Animals potentially face daily exposure to bacterial contamination from these sources.
Nevertheless, LeJeune et al. [172] indicated that the degree of bacterial contamination was associated
with potentially controllable management factors. Water systems in stables represent a complex
ecosystem that is affected by multiple factors. These factors influence the persistence and the effects of
bacteria in drinking water (pipelines and troughs) [172,177]. The multiple factors are diverse: entry
of biomass into the system promotes biofilm growth as a medium for microorganisms, installation
defects, backward spread of bacteria, high temperature, etc. Therefore, it is essential to control the
quality of the animals’ drinking water at regular intervals (at least once a year) [178]. Hartung and
Kamphues [179] determined basic practical and species-specific aspects in housing conditions including
the water collection and distribution system as basic requirements for sustainable livestock and housing
management [178,179]. Heinemann et al. [130] found high bacterial loads in animal drinkers after
cleaning and disinfection, which could lead to a vertical transfer of pathogens to newly arriving
pigs. In this context, Heinemann et al. [130] indicated that decontamination strategies such as
intensive cleaning and disinfection were effective at reducing the levels of Enterobacteriaceae on stable
floors. Nevertheless, residual contamination remains in the environment and on the surfaces of
troughs and drinkers [129,130]. The findings of Jutkina et al. [180] therefore indicate that exposure
to sub-lethal concentrations of certain antimicrobials may contribute to the emerging problem of
antibiotic resistance not only through selection of certain resistance phenotypes, but also by means of
stimulating transfer of antimicrobial resistance traits directly. Schwartz et al. [164] assumed a possible
transfer from wastewater and surface water to drinking water distribution systems. Hölzel et al. [181]
expected that antibiotic-resistant bacteria could also reach the food chain via human and animal
manure applications. Thus, the possible risk for the transmission of antibiotic-resistant bacteria,
resistance genes, and antibiotics from human wastewater or animal manure to the environment,

245
Sustainability 2018, 10, 3967

including drinking waters and the food chain, cannot be neglected. Some studies have reported
multidrug-resistant pathogens in the soil and water of farm environments. The ESBL-variants detected
corresponded to those previously found in animals or humans living in a farm environment [182,183]
(Table S5). To date, several non-European studies have reported multidrug-resistant pathogens in
the vegetables, soil, and water of farm environments. The ESBL-variants detected corresponded to
those previously found in animals or humans living in a farm environment [182,183]. Vital et al. [184]
proved that multidrug-resistant isolates were observed in irrigation water, soil, and vegetables in
urban farms, indicating that water serves as a possible route for a wide distribution across all types
of borders. All of the presented studies commonly demonstrate (molecular) homology analysis of
CTX-M-producing E. coli isolates collected from water and/or swine, and/or human, implying that
multidrug-resistant pathogens in the aquatic environment might derive from both humans and
animals [44,185]. However, contaminated slurry was presented as the major emission source for
ESBL/AmpC-producing E. coli in pig fattening farms [158]. Several other studies identified ESBL
strains in manure samples from pig farms (Table S5). However, a possible link between the prevalence
of ESBL-E in hospitals and other sources such as local food, water, or animal sources has not been
identified [186].

3.5. LA-MRSA and ESBL-E in the Food Chain: Abattoir Biotope

Abattoirs can be possible sources of drug-resistant bacteria [187]: Carry-over of resistant
bacteria at the time of slaughter, the hygiene related to the slaughter processes, meat processing
hygiene, and retail handling [188,189] (Table S6). Pietsch et al. [47] found isolates of distinct
E. coli clonal lineages in all three reservoirs of human, animal, and food in Germany. However,
a direct clonal relationship of isolates from food animals and humans was only noticeable for
a few cases. All foodborne outbreaks have been caused by enteropathogens. The role of the
ESBL-producing Enterobacteriaceae in these persons was considered as commensal flora. Thus, in
comparison to the general population, humans involved in food processing need to be considered
as very important intermediate reservoirs and vectors for ESBL genes remaining in food retailers
contaminated with ESBL-producing bacteria [190]. Normanno et al. [191] clearly demonstrated the
need for improved hygiene standards to reduce the risk of occupational and foodborne infection
linked to the handling/consumption of raw pork containing resistant bacteria like MRSA and
ESBL-Enterobacteriaceae.

4. Sustainable Biotope Approaches

4.1. Animal Health in the Livestock Biotope

The origin of many health problems in pig production is very complex in nature [192]. Diseases
that occur in a multi-factor system such as pig production are not only defined by one factor, but by
the interplay of a variety of processes that take place in the animate and inanimate environments of
the animal and within the animal [192]. Künneken [143] described the interaction between several
factors in the stable environment in his model (Figure 3).
In modern intensive livestock, the following infection-promoting and infection-inhibiting factors
can influence the balance of the stable biotope:

1. A high number of passages of host pathogens with potentially increased virulence within herds;
2. Higher rates of the adhesion of pathogens;
3. The rapid spread of pathogens via direct host contact, food, water, air, and living vectors;
4. The use of high-performance animals that are more sensitive to environmental stressors;
5. The neglect of hygiene principles, e.g., sufficient drying times during cleaning and
disinfection; and
6. The reduced possibility of individual health control and animal observation [143].

246
Sustainability 2018, 10, 3967

Figure 3. Relationships between animate and inanimate factors in environmental reservoirs (modified
according to Künneken [143]).

These infection-promoting and infection-inhibiting factors are involved in constantly changing

processes in the stable biotope. If there is a summation of many infection-promoting factors in one
or all of the three systems, a chain of events is initiated with the possible outcome of an infectious
disease [192]. Walker et al. [193] identified three aspects in the problem of increasing the resistance
of bacteria in, for example, a pig producing system: Pigs have difficulties developing and stabilizing
their individual natural barrier and immune response (stable-specific immunity) against the increase
and spread of pathogens caused by a high pig density or when pigs are introduced into a new stable
with a foreign pig population. These and other actions can trigger chronic stress responses with the
pigs becoming more susceptible to infections that are caused by potentially infectious commensal
bacteria [194]. Thus, closed systems show lower colonization rates with multidrug-resistant bacteria
than those farms with a high rate of incoming pigs (maybe even from one or even more than two
different suppliers), which interferes with stable immunity [10,195]. Thielen et al. [196] referred to
animal health in livestock as a balance between infection pressure and the animals’ immune systems.

4.2. Preventive Health Management: Part of Quality Management

At the beginning of the last century, animals were only treated when they were clearly suffering
from a disease or if their lives were acutely threatened. Whereas in recent decades, the concept
of “integrated veterinary herd health care” has been established, focusing on the combination of
systematic animal health management of the entire animal population for the prevention and early
detection of diseases. Today, the focus is on the implementation to react to any deviation from the
normal state as fast as possible given that diseases, even if they occur without visible symptoms,
impair the well-being of the animals, and thus have effects on eating and drinking behavior [197].
From the perspective of protecting consumer health, it is important to prevent the entry of
pathogens from animal origins that are likely to cause human zoonosis [198]. Strategies for the
maintenance of animal health afford a direct contribution towards optimizing consumer health
protection [199]. In recent years, research projects have focused on the implementation and

247
Sustainability 2018, 10, 3967

organization of intra and inter-farm health management systems in meat-production chains [200–210].
The main task of health management is the maintenance of animal health at all stages of animal
production. Animal health not only has special significance for the production of healthy food,
but also for the economical optimization of the various production stages, namely farrowing, nursery,
and finishing [201,204,205]. According to Berns [200] and Welz [208], diseases are considered as process
errors and quality-reducing effects in terms of quality management. Therefore, preventive quality
management focuses on health precautions on livestock farms [211].
Similar to human medicine, animal health management can be divided into three levels
(Table 1) [212].

Table 1. Definition of the three levels of prevention (according to Schulze Althoff, [212]).

Level Definition
Structural, group-based and individual measures to prevent the
Primary prevention occurrence of disturbances
Preventive measures initiated once the pathogen has been identified in
Secondary prevention order to prevent progression of the disturbance
Measures to prevent aggravation of the disturbance and mitigate the
Tertiary prevention
effects of the disturbance

According to Berns [200], the main priorities of preventive animal health management are the
following:

• Detect diseases while still in the subclinical stage;

• Prevent infections from progressing to a clinical stage and stop the spread from a single animal to
the whole herd; and
• Identify and promptly eliminate stressors and risks to animal health from the environment.

Consequently, to ensure food safety and quality, the traditional quality control at the end of
the production process needs to be supplemented by control inspections at an incoming and at
an intermediate level—when selling and purchasing piglets, finishing pigs, and at slaughter [204].
To assure food safety and consumer protection, only healthy pigs that originate from farms
with a certified health status should be slaughtered [212]. Health and quality assurance in pork
production encompasses:

• Pig supplying farms;

• Networks of primary producers; and
• Slaughtering, processing, and distribution [205,213].

Thus, animal health management is deemed to be an integral part of quality management in

a food supply chain, all the way to grocery retail stores [198,214]. Coordinating these measures
with several enterprises along the value-added pork chain defines the inter-farm chain-oriented
quality management [215]. The concept of a quality management system is defined as systematic
planning, implementation, and documentation with an influence on the quality of a product [206,209].
The driving force is each participating enterprise’s awareness that by improving its own quality
management, it can make the quality management efforts of other enterprises in the value chain
more efficient. This enables the maximization of the profits of the enterprises that compose the value
chain [216,217].

4.3. “One Health” Crossing Biotopes

The interdisciplinary cooperation in solving complex health problems is intended to create
incentives for system innovation [50]. The resistance problem is one of many examples that can be
perfectly addressed within the “One Health” approach [218–221]. In the case of pork production,

248
Sustainability 2018, 10, 3967

this means considering humans and animals in the “livestock” biotope, as well as the “food processing
and transport” and “health care system” biotopes, are all interconnected via the environment.
Every pig production farm that produces animals for sale constitutes a separate biotope. Pigs,
throughout their life, are often moved from one biotope to another. The production of pigs usually
includes four transfers and changes of stables. Each farm involved constitutes a geographical and
organizational unit within the chain [209]. Nevertheless, it should not be underestimated that on
finishing farms, the source of the colonization of pigs, whether acquired at the current stage or
during farrowing or nursery stages, often cannot be determined [222]. De Neeling et al. [222]
and other authors [223,224] have reported that pigs, colonized at the farrowing or nursery farm,
carry their microbial load over to the finishing stage. In this context, the livestock biotope greatly
benefits from inter-farm measures that detect and promptly reduce the risk of infections spreading
from one stage of production to the next [201,214]. The establishment of monitoring systems and
the certification of farms according to their health status use this approach. Hereby, single and
intra and inter-farm audits as well as monitoring for specific pathogens (e.g., for LA-MRSA and
ESBL-E) have been implemented [201,204,205]. With the renewal of the German Drug Act (16th
AMG-Novelle) in 2014, antibiotic consumption in farm animal production is monitored to reduce its
usage. Exceeding the farm-specific biannual therapeutic frequency beyond the 75% quantile obligates
livestock owners to submit a written plan of measures to the public veterinary authority. Four years
after its implementation, an in-depth scientific evaluation of the antibiotic monitoring is still due [225].
Epidemiological trends within a value-added chain can, according to Schulze-Geisthövel et al.
(2015), be recognized, and farm comparisons such as industry marketing can be made by the
common use of investigation data. Salmonella monitoring, for instance, is regularly included in
the coordinated investigations between supplier farms and abattoirs [226,227]. Schulze Althoff [209]
and Düsseldorf [201] stressed that it would make sense along the pig production chain for a receiving
inspection to be referred to the supplier, an intermediate checkup referred to the farm, and a final
inspection referred to the customer. This is because the carcass can be contaminated through the
slaughtering process as well as by the intestinal contents of the slaughtered animals [7]. Therefore,
all E.U. member states are obligated by guideline 2003/99/EG to monitor for zoonosis and zoonotic
bacteria. In the context of zoonosis monitoring, representative data regarding the occurrence of
zoonotic bacteria has for years been acquired in the most important food supplying animal species
and products to measure the infection risk for consumers from consuming food.
Furthermore, many decision-makers in politics and science have demanded and promoted
from agricultural science, veterinarian and human medicine, and environmental sciences, a common
collaborative holistic strategy (the “One Health” approach) against the spread of antibiotic-resistant
bacteria [51,220].

5. Final Remarks, Recommendations and Future Directions

The holistic collaborative “One Health” approach between human medicine and agricultural
sciences has advanced the risk assessment of the dynamics of MRSA and ESBL-E transmission
pathways as well as that of human exposure related to livestock production (particularly pigs) and
processing. The impact of the importance of these “indicator bacteria” is still under debate; especially
as new resistance problems and transferable resistance genes are emerging. For example, the global rise
of Carbapenemase-producing Enterobacteriaceae has resulted in the increased use of Colistin resistance
and is associated with the risk of emerging resistance. This concerns agriculture just as much as human
medicine and requires round table discussions on the prudent and sustainable use of antibiotics on
both sides. As this review has demonstrated, these discussions will no longer only focus on humans
and animals and their food products. The focus of “One Health” will expand and focus on the
environmental aspect. On the other hand, in environmental hotspots with their own dynamics and
links to the reservoirs and vectors, and “animal” and “human” in different biotopes are currently
crystallizing out.

249
Sustainability 2018, 10, 3967

This review tried to make a small contribution to the better understanding of possible transmission
pathways between the presented reservoirs and highlights the following aspects:

- Healthy animals do not need antibiotic medication, thus further suppressing the risk of the
occurrence of non-pathogenic resistant bacteria. The constant administration of antibiotics
to animals will destroy potential antibiotics. Therefore, to save existing potential antibiotics,
the government, physicians, and farm industries should limit the prescription of antibiotics
to prevent antibiotic resistance, and people should not easily obtain access to self-medicated
antibiotics, especially in developing countries.
- Farmers and veterinarians come into contact with antimicrobial-resistant bacteria from pigs
within the stable environment. Strong associations between the isolation of resistant commensal
bacteria (both MRSA and ESLB-E) and contact with pigs and even the working hours in the stable
could be made.
- However, not only do animals present potential reservoirs or vectors for transferring resistance
genes and resistant bacteria, but even farmers and farm workers themselves should also be
considered for their transmission potential.
- Thus, aside from organic factors, the inanimate environment such as the stable climate has a
substantial influence on the well-being and health status of pigs and the tenacity of bacteria.
Air and dust were clearly determined as sources for the contamination of humans and animals
mainly with MRSA.
- Wastewater in general (municipal, urban, with clinical and/or agroindustrial influence) serves as
a melting pot for the possible horizontal transfer between resistance genes and multidrug-resistant
bacteria. Whereas the impact of animal wastewater on surface water has yet to be investigated.

Thus far, resistant bacteria could be isolated with a higher percentage from swine and
slaughterhouse wastewater, only indicating the potential role of agricultural wastewater within the
context of environmental resistance pollution.

- Many resistant bacteria in animal drinkers could be identified after cleaning and disinfection,
which could lead to a vertical transfer of pathogens to newly arriving pigs. Therefore, methods for
cleaning performances, especially regarding the water systems in pig stables, should be evaluated.
- A high prevalence of ESBL-E was found in pig manure, indicating a high emission and
transmission potential into the stable environment and their surroundings.
- Contamination of meat with ESBL-producing E. coli and MRSA is no longer surprising. However,
the growing diversity of ESBL-E indicates a growing dissemination of ESBL-genes in E. coli in
meat products from porcine origin.

Some aspects could improve our ability to mitigate the spread of resistances and would be a
useful supplement to the already existing health management initiatives. Possible strategies for
the enhancement of individual defense mechanisms and control of the resistance status could be
the following:

• Limit the purchase of new pigs to those that are accompanied with health certificates from the
supply farms.
• Determine the MRSA/ESBL status (similar to the Salmonella monitoring), take part in a continued
health-monitoring program and create financial incentives for reduction measures.
• Use workshops and training to transfer scientific knowledge and sensitize for reduction measures.

However, permanent colonization should be distinguished from transient colonization.

Interventions—as already implemented in the health care system—may prevent transient colonization
and may hence be a useful control of MRSA not only in the hospital, but also in the stable environment.

250
Sustainability 2018, 10, 3967

In general, knowledge and information about the biotope-crossing potential of multidrug-resistant

bacteria and antibiotic resistances should be the most important approach within the “One Health”
concept. Several articles in this review demonstrated that these aspects are not yet anchored in
the teaching and education of farmers, (medical and agriculture) students, multipliers, and policy
makers. In summary, these approaches contribute to a larger goal of achieving the early recognition
of antimicrobial resistance in bacterial livestock pathogens. Therefore, future scientific efforts should
clarify the persistence and spread of highly resistant bacteria in the environment, especially in the
stable and aquatic environment and their interface.
Within this framework, the implications of the “One Health” approach could have a positive
impact on all sustainable future strategies.

Supplementary Materials: The following are available online at http://www.mdpi.com/2071-1050/10/11/3967/s1.

Table S1: Discussion of eight factors possibly influencing transmission and bioavailability of drug-resistant
bacteria. Table S2: Overview of LA-MRSA and ESBL-E in humans in the stable biotope. Abbreviations for the
transmission pathways: HH = Human to Human, AA = Animal to Animal, HA = Human to Animal, AH = Animal
to Human, HE = Human to Environment, EH = Environment to Human, AE = Animal to Environment,
EA = Environment to Animal, EE = Environment to Environment, FH = Food to Human, HF = Human to
Food, EF = Environment to Food, AF = Animal to Food. Abbreviations for the countries: NL = Netherlands,
ESP = Spain, IT = Italy, EU = Europe, DEN = Denmark, UK = United Kingdom, GER = Germany, BEL = Belgium,
FR = France, USA = United States of America, CHE = Switzerland, HKG = Hong Kong. Table S3: Overview over
several studies describing the different possibilities of the transmission of antibiotic-resistant bacteria (MRSA and
ESBL-E) between pigs. Abbreviations for the transmission pathways: HH = Human to Human, AA = Animal to
Animal, HA = Human to Animal, AH = Animal to Human, HE = Human to Environment, EH = Environment
to Human, AE = Animal to Environment, EA = Environment to Animal, EE = Environment to Environment,
FH = Food to Human, HF = Human to Food, EF = Environment to Food, AF = Animal to Food. Abbreviations
for the countries: NL = Netherlands, ESP = Spain, IT = Italy, EU = Europe, DEN = Denmark, UK = United
Kingdom, GER = Germany, BEL = Belgium, FR = France, USA = United States of America, CHE = Switzerland,
INT = international (worldwide). Table S4: Overview of LA-MRSA and ESBL-E in air and dust in the stable
environment. Abbreviations for the transmission pathways: HH = Human to Human, AA = Animal to Animal,
HA = Human to Animal, AH = Animal to Human, HE = Human to Environment, EH = Environment to
Human, AE = Animal to Environment, EA = Environment to Animal, EE = Environment to Environment,
FH = Food to Human, HF = Human to Food, EF = Environment to Food, AF = Animal to Food. Abbreviations
for the countries: HUN = Hungary, NL = Netherlands, ESP = Spain, IT = Italy, EU = Europe, CHN = China,
NOR =Norway, DEN = Denmark, UK = United Kingdom, GER = Germany, BEL = Belgium, FR = France,
USA = United States of America, CHE = Switzerland. Table S5: Table overview over LA-MRSA and ESBL-E
in Water, Wastewater and Manure of pig production facilities. Abbreviations for the transmission pathways:
HH = Human to Human, AA = Animal to Animal, HA = Human to Animal, AH = Animal to Human, HE = Human
to Environment, EH = Environment to Human, AE = Animal to Environment, EA = Environment to Animal,
EE = Environment to Environment, FH = Food to Human, HF = Human to Food, EF = Environment to Food,
AF = Animal to Food. Abbreviations for the countries: NL = Netherlands, ESP = Spain, IT = Italy, EU = Europe,
CHN = China, NOR = Norway, DEN = Denmark, UK = United Kingdom, GER = Germany, BEL = Belgium,
FR = France, USA = United States of America, CHE = Switzerland, PHL = Philippines. Table S6: Table overview
over LA-MRSA and ESBL-E in the Food Chain: Abattoir Biotope and Human vectors in Pig Meat Processing.
Abbreviations for the transmission pathways: HH = Human to Human, AA = Animal to Animal, HA = Human to
Animal, AH = Animal to Human, HE = Human to Environment, EH = Environment to Human, AE = Animal
to Environment, EA = Environment to Animal, EE = Environment to Environment, FH = Food to Human,
HF = Human to Food, EF = Environment to Food, AF = Animal to Food. Abbreviations for the countries:
CAN = Canada, NL = Netherlands, ESP = Spain, IT = Italy, EU = Europe, CHN = China, NOR = Norway,
DEN = Denmark, UK = United Kingdom, GER = Germany, BEL = Belgium, FR = France, USA = United States of
America, CHE = Switzerland, JAP = Japan, AUS = Austria.
Author Contributions: Each author made substantial contributions to: Conceptualisation: R.M.S., S.V.S.-G., G.B.,
M.E. and B.P.; Formal analysis: R.M.S. and J.S.-W.; Investigation: R.M.S. and S.V.S.-G.; Methodology: R.M.S,
S.V.S.-G. and C.H.; Project administration: R.M.S. and B.P.; Supervision: M.E.; Validation: R.M.S and J.S.-W.;
Visualization: R.M.S. and S.V.S.-G.; Writing—original draft: R.M.S.; Writing—review & editing: R.M.S., C.H., G.B.
and J.S.-W.
Funding: “This research received no external funding” at the Institute of Animal Sciences at the University of
Bonn and the Institutes of Medical Microbiology, Immunology and Parasitology, Hygiene and Public Health at
the University Hospital Bonn.
Conflicts of Interest: The authors declare no conflict of interest.

251
Sustainability 2018, 10, 3967

References
1. Gilchrist, M.J.; Greko, C.; Wallinga, D.B.; Beran, G.W.; Riley, D.G.; Thorne, P.S. The potential role
of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance.
Environ. Health Perspect. 2007, 115, 313–316. [CrossRef] [PubMed]
2. Mathew, A.G.; Cissell, R.; Liamthong, S. Antibiotic resistance in bacteria associated with food animals:
A United States perspective of livestock production. Foodborne Pathog. Dis. 2007, 4, 115–133. [CrossRef]
[PubMed]
3. Threlfall, E.J.; Ward, L.R.; Frost, J.A.; Willshaw, G.A. The emergence and spread of antibiotic resistance in
food-borne bacteria. Int. J. Food Microbiol. 2000, 62, 1–5. [CrossRef]
4. Pruden, A.; Larsson, D.G.; Amézquita, A.; Collignon, P.; Brandt, K.K.; Graham, D.W.; Lazorchak, J.M.;
Suzuki, S.; Silley, P.; Snape, J.R.; et al. Management options for reducing the release of antibiotics and
antibiotic resistance genes to the environment. Environ. Health Perspect. 2013, 121, 878–885. [CrossRef]
[PubMed]
5. Landers, T.F.; Cohen, B.; Wittum, T.E.; Larson, E.L. A review of antibiotic use in food animals: Perspective,
policy, and potential. Public Health Rep. 2012, 127, 4–22. [CrossRef] [PubMed]
6. Escudero, E.; Vinué, L.; Teshager, T.; Torres, C.; Moreno, M.A. Resistance mechanisms and farm-level
distribution of fecal Escherichia coli isolates resistant to extended-spectrum cephalosporins in pigs in Spain.
Res. Vet. Sci. 2010, 88, 83–87. [CrossRef] [PubMed]
7. Hansen, K.H.; Damborg, P.; Andreasen, M.; Nielsen, S.S.; Guardabassi, L. Carriage and fecal counts of
cefotaxime M-producing Escherichia coli in pigs: A longitudinal study. Appl. Environ. Microbiol. 2013,
79, 794–798. [CrossRef] [PubMed]
8. Broens, E.M.; Graat, E.A.; Van der Wolf, P.J.; Van de Giessen, A.W.; De Jong, M.C. Transmission of methicillin
resistant Staphylococcus aureus among pigs during transportation from farm to abattoir. Vet. J. 2011,
189, 302–305. [CrossRef] [PubMed]
9. Broens, E.M.; Graat, E.A.; van der Wolf, P.J.; van de Giessen, A.W.; van Duijkeren, E.; Wagenaar, J.A.; van
Nes, A.; Mevius, D.J.; de Jong, M.C. MRSA CC398 in the pig production chain. Prev. Vet. Med. 2011,
98, 182–189. [CrossRef] [PubMed]
10. van Duijkeren, E.; Ikawaty, R.; Broekhuizen-Stins, M.J.; Jansen, M.D.; Spalburg, E.C.; de Neeling, A.J.;
Allaart, J.G.; van Nes, A.; Wagenaar, J.A.; Fluit, A.C. Transmission of methicillin-resistant Staphylococcus
aureus strains between different kinds of pig farms. Vet. Microbiol. 2008, 126, 383–389. [CrossRef] [PubMed]
11. Schulze-Geisthövel, S.; Schmithausen, R.; Stemmer, F.; El-Sade, M.; Hoerauf, A.; Exner, M.; Bierbaum, G.;
Bekeredjian-Ding, I.; Petersen, B. Occurrence of MRSA and ESBL in different habitats and different stages
of the pork production chain. In Proceedings of the DACH Epidemiologietagung “Tiergesundheit und
Ökonomie”, Zürich, Schweiz, 3–5 September 2014.
12. Hunter, P.A.; Dawson, S.; French, G.L.; Goossens, H.; Hawkey, P.M.; Kuijper, E.J.; Nathwani, D.; Taylor, D.J.;
Teale, C.J.; Warren, R.E.; et al. Antimicrobial-resistant pathogens in animals and man: Prescribing, practices
and policies. J. Antimicrob. Chemother. 2010, 65 (Suppl. 1), i3–i17. [CrossRef] [PubMed]
13. Hawkey, P.M.; Jones, A.M. The changing epidemiology of resistance. J. Antimicrob. Chemother. 2009, 64
(Suppl. 1), i3–i10. [CrossRef] [PubMed]
14. Li, X.Z.; Mehrotra, M.; Ghimire, S.; Adewoye, L. Beta-Lactam resistance and beta-lactamases in bacteria of
animal origin. Vet. Microbiol. 2007, 121, 197–214. [CrossRef] [PubMed]
15. Müller, A.; Stephan, R.; Nüesch-Inderbinen, M. Distribution of virulence factors in ESBL-producing
Escherichia coli isolated from the environment, livestock, food and humans. Sci. Total Environ. 2016,
541, 667–672. [CrossRef] [PubMed]
16. Westphal-Settele, K.; Konradi, S.; Balzer, F.; Schönfeld, J.; Schmithausen, R. The environment as a reservoir for
antimicrobial resistance: A growing problem for public health? Bundesgesundheitsblatt Gesundheitsforschung
Gesundheitsschutz 2018, 61, 533–542. [CrossRef] [PubMed]
17. Mehndiratta, P.L.; Bhalla, P. Use of antibiotics in animal agriculture & emergence of methicillin-resistant
Staphylococcus aureus (MRSA) clones: Need to assess the impact on public health. Indian J. Med. Res. 2014,
140, 339–344. [PubMed]

252
Sustainability 2018, 10, 3967

18. Liverani, M.; Waage, J.; Barnett, T.; Pfeiffer, D.U.; Rushton, J.; Rudge, J.W.; Loevinsohn, M.E.; Scoones, I.;
Smith, R.D.; Cooper, B.S.; et al. Understanding and managing zoonotic risk in the new livestock industries.
Environ. Health Perspect. 2013, 121, 873–877. [CrossRef] [PubMed]
19. Mather, A.E.; Matthews, L.; Mellor, D.J.; Reeve, R.; Denwood, M.J.; Boerlin, P.; Reid-Smith, R.J.; Brown, D.J.;
Coia, J.E.; Browning, L.M.; et al. An ecological approach to assessing the epidemiology of antimicrobial
resistance in animal and human populations. Proc. Biol. Sci. 2012, 279, 1630–1639. [CrossRef] [PubMed]
20. EFSA. Assessment of the Public Health Significance of Methicillin Resistant Staphylococcus Aureus (MRSA) in
Animals and Foods; EFSA: Parma, Italy, 2009.
21. Da Costa, P.M.; Loureiro, L.; Mator, A.J.F. Transfer of multidrug-resistant bacteria between intermingled
ecological niches: The interface between humans, animals and the environment. Int. J. Environ. Res.
Public Health 2013, 10, 278–294. [CrossRef] [PubMed]
22. BfR. ESBL-Bildende Bakterien in Lebensmitteln und Deren Übertragbarkeit auf den Menschen; Bundesinstitut für
Risikobewertung (BfR): Berlin, Germany, 2010.
23. Willyard, C. The drug-resistant bacteria that pose the greatest health threats. Nature 2017, 543, 15. [CrossRef]
[PubMed]
24. Guenther, S.; Ewers, C.; Wieler, L.H. Extended-spectrum beta-lactamases producing E. coli in wildlife, yet
another form of environmental pollution? Front. Microbiol. 2011, 2, 246. [CrossRef] [PubMed]
25. Cuny, C.; Nathaus, R.; Layer, F.; Strommenger, B.; Altmann, D.; Witte, W. Nasal colonization of humans with
methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS ONE
2009, 4, e6800. [CrossRef] [PubMed]
26. Deiters, C.; Günnewig, V.; Friedrich, A.W.; Mellmann, A.; Köck, R. Are cases of Methicillin-resistant
Staphylococcus aureus clonal complex (CC) 398 among humans still livestock-associated? Int. J.
Med. Microbiol. 2015, 305, 110–113. [CrossRef] [PubMed]
27. Van den Bogaard, A.E.; Stobberingh, E.E. Epidemiology of resistance to antibiotics. Links between animals
and humans. Int. J. Antimicrob. Agents 2000, 14, 327–335. [CrossRef]
28. Marshall, B.M.; Levy, S.B. Food animals and antimicrobials: Impacts on human health. Clin. Microbiol. Rev.
2011, 24, 718–733. [CrossRef] [PubMed]
29. Aarestrup, F.M.; Hasman, H.; Agersø, Y.; Jensen, L.B.; Harksen, S.; Svensmark, B. First description of
blaCTX-M-1-carrying Escherichia coli isolates in Danish primary food production. J. Antimicrob. Chemother.
2006, 57, 1258–1259. [CrossRef] [PubMed]
30. Liebana, E.; Batchelor, M.; Hopkins, K.L.; Clifton-Hadley, F.A.; Teale, C.J.; Foster, A.; Barker, L.;
Threlfall, E.J.; Davies, R.H. Longitudinal farm study of extended-spectrum beta-lactamase-mediated
resistance. J. Clin. Microbiol. 2006, 44, 1630–1634. [CrossRef] [PubMed]
31. De Boer, E.; Zwartkruis-Nahuis, J.T.; Wit, B.; Huijsdens, X.W.; de Neeling, A.J.; Bosch, T.; van Oosterom, R.A.;
Vila, A.; Heuvelink, A.E. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int. J.
Food Microbiol. 2009, 134, 52–56. [CrossRef] [PubMed]
32. Wulf, M.W.; Verduin, C.M.; van Nes, A.; Huijsdens, X.; Voss, A. Infection and colonization with methicillin
resistant Staphylococcus aureus ST398 versus other MRSA in an area with a high density of pig farms. Eur. J.
Clin. Microbiol. Infect. Dis. 2012, 31, 61–65. [CrossRef] [PubMed]
33. Van Cleef, B.A.; Verkade, E.J.; Wulf, M.W.; Buiting, A.G.; Voss, A.; Huijsdens, X.W.; van Pelt, W.;
Mulders, M.N.; Kluytmans, J.A. Prevalence of livestock-associated MRSA in communities with high
pig-densities in The Netherlands. PLoS ONE 2010, 5, e9385. [CrossRef] [PubMed]
34. Monaco, M.; Pedroni, P.; Sanchini, A.; Bonomini, A.; Indelicato, A.; Pantosti, A. Livestock-associated
methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of
Italy with high density of pig farming. BMC Infect. Dis. 2013, 13, 258. [CrossRef] [PubMed]
35. Aubry-Damon, H.; Grenet, K.; Sall-Ndiaye, P.; Che, D.; Cordeiro, E.; Bougnoux, M.E.; Rigaud, E.; Le Strat, Y.;
Lemanissier, V.; Armand-Lefèvre, L.; et al. Antimicrobial resistance in commensal flora of pig farmers.
Emerg. Infect. Dis. 2004, 10, 873–879. [CrossRef] [PubMed]
36. Köck, R.; Schaumburg, F.; Mellmann, A.; Köksal, M.; Jurke, A.; Becker, K.; Friedrich, A.W.
Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection
and colonization in Germany. PLoS ONE 2013, 8, e55040. [CrossRef] [PubMed]

253
Sustainability 2018, 10, 3967

37. Köck, R.; Bischoff, M.; Cuny, C.; Eckmanns, T.; Fetsch, A.; Harmsen, D.; Goerge, T.; Oberheitmann, B.;
Schwarz, S.; Selhorst, T.; et al. The burden of zoonotic MRSA colonization and infection in Germany.
Berl. Munch. Tierarztl. Wochenschr. 2014, 127, 384–398. [PubMed]
38. Bisdorff, B.; Scholhölter, J.L.; Claußen, K.; Pulz, M.; Nowak, D.; Radon, K. MRSA-ST398 in livestock farmers
and neighbouring residents in a rural area in Germany. Epidemiol. Infect. 2012, 140, 1800–1808. [CrossRef]
[PubMed]
39. Johnson, J.R.; Kuskowski, M.A.; Smith, K.; O’Bryan, T.T.; Tatini, S. Antimicrobial-resistant and extraintestinal
pathogenic Escherichia coli in retail foods. J. Infect. Dis. 2005, 191, 1040–1049. [CrossRef] [PubMed]
40. Overdevest, I.; Willemsen, I.; Rijnsburger, M.; Eustace, A.; Xu, L.; Hawkey, P.; Heck, M.; Savelkoul, P.;
Vandenbroucke-Grauls, C.; van der Zwaluw, K.; et al. Extended-spectrum β-lactamase genes of Escherichia
coli in chicken meat and humans, The Netherlands. Emerg. Infect. Dis. 2011, 17, 1216–1222. [CrossRef]
[PubMed]
41. Jakobsen, L.; Spangholm, D.J.; Pedersen, K.; Jensen, L.B.; Emborg, H.D.; Agersø, Y.; Aarestrup, F.M.;
Hammerum, A.M.; Frimodt-Møller, N. Broiler chickens, broiler chicken meat, pigs and pork as sources of
ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans
and UTI patients. Int. J. Food Microbiol. 2010, 142, 264–272. [CrossRef] [PubMed]
42. Weese, J.S.; Rousseau, J. Attempted eradication of methicillin-resistant staphylococcus aureus colonisation in
horses on two farms. Equine Vet. J. 2005, 37, 510–514. [CrossRef] [PubMed]
43. Friese, A.; Schulz, J.; Hoehle, L.; Fetsch, A.; Tenhagen, B.A.; Hartung, J.; Roesler, U. Occurrence of MRSA in
air and housing environment of pig barns. Vet. Microbiol. 2012, 158, 129–135. [CrossRef] [PubMed]
44. Hu, Y.Y.; Cai, J.C.; Zhou, H.W.; Chi, D.; Zhang, X.F.; Chen, W.L.; Zhang, R.; Chen, G.X. Molecular typing of
CTX-M-producing escherichia coli isolates from environmental water, swine feces, specimens from healthy
humans, and human patients. Appl. Environ. Microbiol. 2013, 79, 5988–5996. [CrossRef] [PubMed]
45. Blake, D.P.; Hillman, K.; Fenlon, D.R.; Low, J.C. Transfer of antibiotic resistance between commensal and
pathogenic members of the Enterobacteriaceae under ileal conditions. J. Appl. Microbiol. 2003, 95, 428–436.
[CrossRef] [PubMed]
46. Martinez, J.L. The role of natural environments in the evolution of resistance traits in pathogenic bacteria.
Proc. Biol. Sci. 2009, 276, 2521–2530. [CrossRef] [PubMed]
47. Pietsch, M.; Irrgang, A.; Roschanski, N.; Brenner Michael, G.; Hamprecht, A.; Rieber, H.; Käsbohrer, A.;
Schwarz, S.; Rösler, U.; Kreienbrock, L.; et al. Whole genome analyses of CMY-2-producing Escherichia coli
isolates from humans, animals and food in Germany. BMC Genom. 2018, 19, 601. [CrossRef] [PubMed]
48. Hammerum, A.M.; Heuer, O.E. Human health hazards from antimicrobial-resistant Escherichia coli of animal
origin. Clin. Infect. Dis. 2009, 48, 916–921. [CrossRef] [PubMed]
49. Wilcox, B.; Kueffer, C. Transdisciplinarity in EcoHealth: Status and future prospects. Ecohealth 2008, 5, 1–3.
[CrossRef] [PubMed]
50. Zinsstag, J.; Schelling, E.; Waltner-Toews, D.; Tanner, M. From “one medicine” to “one health” and systemic
approaches to health and well-being. Prev. Vet. Med. 2011, 101, 148–156. [CrossRef] [PubMed]
51. Haxton, E.; Sinigoj, S.; Betson, M.; Riviere-Cinnamond, A. Evidence-based added value of One Health: The
Network for Evaluation of One Health (NEOH). One Health Sweden 2015. Available online: http://neoh.
onehealthglobal.net/wp-content/uploads/sites/2/2015/01/NEOH-UPDATES-NOV-2015.pdf (accessed
on 23 October 2018). [CrossRef] [PubMed]
52. Köck, R.; Kreienbrock, L.; van Duijkeren, E.; Schwarz, S. Antimicrobial resistance at the interface of human
and veterinary medicine. Vet. Microbiol. 2017, 200, 1–5. [CrossRef] [PubMed]
53. Denis, O.; Suetens, C.; Hallin, M.; Catry, B.; Ramboer, I.; Dispas, M.; Willems, G.; Gordts, B.; Butaye, P.;
Struelens, M.J. Methicillin-resistant Staphylococcus aureus ST398 in swine farm personnel, Belgium.
Emerg. Infect. Dis. 2009, 15, 1098–1101. [CrossRef] [PubMed]
54. Alanis, A.J. Resistance to antibiotics: Are we in the post-antibiotic era? Arch. Med. Res. 2005, 36, 697–705.
[CrossRef] [PubMed]
55. Smet, A.; Martel, A.; Persoons, D.; Dewulf, J.; Heyndrickx, M.; Herman, L.; Haesebrouck, F.; Butaye, P.
Broad-spectrum β-lactamases among Enterobacteriaceae of animal origin: Molecular aspects, mobility and
impact on public health. FEMS Microbiol. Rev. 2010, 34, 295–316. [CrossRef] [PubMed]

254
Sustainability 2018, 10, 3967

56. GERMAP. GERMAPAntibiotikaresistenz und -verbrauchBericht über den Antibiotikaverbrauch und die
Verbreitung von Antibiotikaresistenzen in der Human- und VeterinÄrmedizin in Deutschland; GERMAP/PEG:
Langen, Germany, 2015.
57. BMEL. Lagebild zum Antibiotikaeinsatz; BMELV: Bonn, Germany, 2017.
58. BVL. Zweite Datenerhebung zur Antibiotikagabe in der Tiermedizin; BVL: Berlin, Germany, 2017.
59. Callens, B.; Persoons, D.; Maes, D.; Laanen, M.; Postma, M.; Boyen, F.; Haesebrouck, F.; Butaye, P.; Catry, B.;
Dewulf, J. Prophylactic and metaphylactic antimicrobial use in Belgian fattening pig herds. Prev. Vet. Med.
2012, 106, 53–62. [CrossRef] [PubMed]
60. Economou, V.; Gousia, P. Agriculture and food animals as a source of antimicrobial-resistant bacteria.
Infect. Drug Resist. 2015, 8, 49–61. [CrossRef] [PubMed]
61. Trolldernier, H. Zu Grundlagen der Antibiotikaresistenz. Mh Vet. Med. 1975, 41, 234–237.
62. Hering, J.; Hille, K.; Frömke, C.; von Münchhausen, C.; Hartmann, M.; Schneider, B.; Friese, A.; Roesler, U.;
Merle, R.; Kreienbrock, L. Prevalence and potential risk factors for the occurrence of cefotaxime resistant
Escherichia coli in German fattening pig farms—A cross-sectional study. Prev. Vet. Med. 2014, 116, 129–137.
[CrossRef] [PubMed]
63. Gothe, C.; Petersen, B. Qualitätsmerkmal Tierwohl; Rhenish Friedrich-Wilhelms University: Bonn, Germany,
2018.
64. TierSchG. Tierschutzgesetz in der Fassung der Bekanntmachung vom 18. Mai 2006. (BGBl. I S. 1206,
1313), das Zuletzt Durch Artikel 141 des Gesetzes vom. März 2017 (BGBl. I S. 626) Geändert Worden
ist. 1972. Available online: https://www.tierhyg.vetmed.uni-muenchen.de/tierschutz/tierschutzlinks/ts_
downloads/tschg.pdf (accessed on 23 October 2018).
65. Bollwahn, W. Grauer Arzneimittelmarkt. Aufklären, keine neuen Gesetze. Top Agrar 1981, 9, 63–67.
66. Aarestrup, F. Sustainable farming: Get pigs off antibiotics. Nature 2012, 486, 465–466. [CrossRef] [PubMed]
67. Quinn, P.; Markey, B.; ME, C.; Donnelly, W.; Leonard, C. Veterinary Microbiology and Microbial Disease;
Blackwell Sciences Ltd.: Oxford, UK, 2002.
68. Kenner, J.; O’Connor, T.; Piantanida, N.; Fishbain, J.; Eberly, B.; Viscount, H.; Uyehara, C.; Hospenthal, D.
Rates of carriage of methicillin-resistant and methicillin-susceptible Staphylococcus aureus in an outpatient
population. Infect. Control Hosp. Epidemiol. 2003, 24, 439–444. [CrossRef] [PubMed]
69. Ito, T.; Okuma, K.; Ma, X.X.; Yuzawa, H.; Hiramatsu, K. Insights on antibiotic resistance of Staphylococcus
aureus from its whole genome: Genomic island SCC. Drug Resist. Updat. 2003, 6, 41–52. [CrossRef]
70. Hiramatsu, K.; Cui, L.; Kuroda, M.; Ito, T. The emergence and evolution of methicillin-resistant
Staphylococcus aureus. Trends Microbiol. 2001, 9, 486–493. [CrossRef]
71. Pinho, M.G.; Filipe, S.R.; de Lencastre, H.; Tomasz, A. Complementation of the essential peptidoglycan
transpeptidase function of penicillin-binding protein 2 (PBP2) by the drug resistance protein PBP2A in
Staphylococcus aureus. J. Bacteriol. 2001, 183, 6525–6531. [CrossRef] [PubMed]
72. Alm, R.A.; McLaughlin, R.E.; Kos, V.N.; Sader, H.S.; Iaconis, J.P.; Lahiri, S.D. Analysis of Staphylococcus
aureus clinical isolates with reduced susceptibility to ceftaroline: An epidemiological and structural
perspective. J. Antimicrob. Chemother. 2014, 69, 2065–2075. [CrossRef] [PubMed]
73. Moisan, H.; Pruneau, M.; Malouin, F. Binding of ceftaroline to penicillin-binding proteins of Staphylococcus
aureus and Streptococcus pneumoniae. J. Antimicrob. Chemother. 2010, 65, 713–716. [CrossRef] [PubMed]
74. Lovering, A.L.; Gretes, M.C.; Safadi, S.S.; Danel, F.; de Castro, L.; Page, M.G.; Strynadka, N.C.
Structural insights into the anti-methicillin-resistant Staphylococcus aureus (MRSA) activity of ceftobiprole.
J. Biol. Chem. 2012, 287, 32096–32102. [CrossRef] [PubMed]
75. De Lencastre, H.; Chung, M.; Westh, H. Archaic strains of methicillin-resistant Staphylococcus aureus:
Molecular and microbiological properties of isolates from the 1960s in Denmark. Microb. Drug Resist. 2000,
6, 1–10. [CrossRef] [PubMed]
76. Jevons, M.P. “Celbenin” resistant staphylococci. Br. Med. J. 1961, 1, 124–125. [CrossRef]
77. Devriese, L.A.; Van Damme, L.R.; Fameree, L. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains
isolated from bovine mastitis cases. Zentralbl. Veterinarmed. B 1972, 19, 598–605. [CrossRef] [PubMed]
78. Price, L.B.; Stegger, M.; Hasman, H.; Aziz, M.; Larsen, J.; Andersen, P.S.; Pearson, T.; Waters, A.E.; Foster, J.T.;
Schupp, J.; et al. Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in
livestock. MBio 2012, 3. [CrossRef] [PubMed]

255
Sustainability 2018, 10, 3967

79. Catry, B.; Van Duijkeren, E.; Pomba, M.C.; Greko, C.; Moreno, M.A.; Pyörälä, S.; Ruzauskas, M.; Sanders, P.;
Threlfall, E.J.; Ungemach, F.; et al. Reflection paper on MRSA in food-producing and companion animals:
Epidemiology and control options for human and animal health. Epidemiol. Infect. 2010, 138, 626–644.
[CrossRef] [PubMed]
80. Witte, W.; Strommenger, B.; Stanek, C.; Cuny, C. Methicillin-resistant Staphylococcus aureus ST398 in humans
and animals, Central Europe. Emerg. Infect. Dis. 2007, 13, 255–258. [CrossRef] [PubMed]
81. Fitzgerald, J.R. Livestock-associated Staphylococcus aureus: Origin, evolution and public health threat.
Trends Microbiol. 2012, 20, 192–198. [CrossRef] [PubMed]
82. Cuny, C.; Friedrich, A.; Kozytska, S.; Layer, F.; Nübel, U.; Ohlsen, K.; Strommenger, B.; Walther, B.; Wieler, L.;
Witte, W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J.
Med. Microbiol. 2010, 300, 109–117. [CrossRef] [PubMed]
83. Lowder, B.V.; Guinane, C.M.; Ben Zakour, N.L.; Weinert, L.A.; Conway-Morris, A.; Cartwright, R.A.;
Simpson, A.J.; Rambaut, A.; Nübel, U.; Fitzgerald, J.R. Recent human-to-poultry host jump, adaptation,
and pandemic spread of Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 2009, 106, 19545–19550.
[CrossRef] [PubMed]
84. Bradford, P.A. Extended-spectrum beta-lactamases in the 21st century: Characterization, epidemiology,
and detection of this important resistance threat. Clin. Microbiol. Rev. 2001, 14, 933–951. [CrossRef] [PubMed]
85. Bradford, P.A.; Petersen, P.J.; Fingerman, I.M.; White, D.G. Characterization of expanded-spectrum
cephalosporin resistance in E. coli isolates associated with bovine calf diarrhoeal disease.
J. Antimicrob. Chemother. 1999, 44, 607–610. [CrossRef] [PubMed]
86. Bradford, P.A.; Urban, C.; Mariano, N.; Projan, S.J.; Rahal, J.J.; Bush, K. Imipenem resistance in Klebsiella
pneumoniae is associated with the combination of ACT-1, a plasmid-mediated AmpC beta-lactamase,
and the foss of an outer membrane protein. Antimicrob. Agents Chemother. 1997, 41, 563–569. [CrossRef]
[PubMed]
87. Paterson, D.L.; Mulazimoglu, L.; Casellas, J.M.; Ko, W.C.; Goossens, H.; Von Gottberg, A.; Mohapatra, S.;
Trenholme, G.M.; Klugman, K.P.; McCormack, J.G.; et al. Epidemiology of ciprofloxacin resistance and its
relationship to extended-spectrum beta-lactamase production in Klebsiella pneumoniae isolates causing
bacteremia. Clin. Infect. Dis. 2000, 30, 473–478. [CrossRef] [PubMed]
88. Kaase, M. Carbapenemases in gram-negative bacteria. Current data and trends of resistance resulting from
the work of national reference centres. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2012,
55, 1401–1404. [CrossRef] [PubMed]
89. Walsh, T.R. Emerging carbapenemases: A global perspective. Int. J. Antimicrob. Agents 2010, 36 (Suppl. 3),
S8–S14. [CrossRef]
90. Patel, G.; Bonomo, R.A. Status report on carbapenemases: Challenges and prospects. Expert Rev. Anti Infect.
Ther. 2011, 9, 555–570. [CrossRef] [PubMed]
91. Livermore, D.M. Beta-Lactamases in laboratory and clinical resistance. Clin. Microbiol. Rev. 1995, 8, 557–584.
[CrossRef] [PubMed]
92. Tham, J.; Walder, M.; Melander, E.; Odenholt, I. Prevalence of extended-spectrum beta-lactamase-producing
bacteria in food. Infect. Drug Resist. 2012, 5, 143–147. [CrossRef] [PubMed]
93. Pitout, J.D. Infections with extended-spectrum beta-lactamase-producing enterobacteriaceae: Changing
epidemiology and drug treatment choices. Drugs 2010, 70, 313–333. [CrossRef] [PubMed]
94. Naseer, U.; Sundsfjord, A. The CTX-M conundrum: Dissemination of plasmids and Escherichia coli clones.
Microb. Drug Resist. 2011, 17, 83–97. [CrossRef] [PubMed]
95. Pitout, J.D.; Gregson, D.B.; Church, D.L.; Elsayed, S.; Laupland, K.B. Community-wide outbreaks of
clonally related CTX-M-14 beta-lactamase-producing Escherichia coli strains in the Calgary health region.
J. Clin. Microbiol. 2005, 43, 2844–2849. [CrossRef] [PubMed]
96. Smet, A.; Martel, A.; Persoons, D.; Dewulf, J.; Heyndrickx, M.; Catry, B.; Herman, L.; Haesebrouck, F.;
Butaye, P. Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal
Escherichia coli Isolates in Belgian broiler farms. Antimicrob. Agents Chemother. 2008, 52, 1238–1243.
[CrossRef] [PubMed]

256
Sustainability 2018, 10, 3967

97. Tian, G.B.; Wang, H.N.; Zou, L.K.; Tang, J.N.; Zhao, Y.W.; Ye, M.Y.; Tang, J.Y.; Zhang, Y.; Zhang, A.Y.;
Yang, X.; et al. Detection of CTX-M-15, CTX-M-22, and SHV-2 extended-spectrum beta-lactamases (ESBLs)
in Escherichia coli fecal-sample isolates from pig farms in China. Foodborne Pathog. Dis. 2009, 6, 297–304.
[CrossRef] [PubMed]
98. Geser, N.; Stephan, R.; Korczak, B.M.; Beutin, L.; Hächler, H. Molecular identification of
extended-spectrum-β-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in
Switzerland. Antimicrob. Agents Chemother. 2012, 56, 1609–1612. [CrossRef] [PubMed]
99. Kiiru, J.; Kariuki, S.; Goddeeris, B.M.; Butaye, P. Analysis of β-lactamase phenotypes and carriage of selected
β-lactamase genes among Escherichia coli strains obtained from Kenyan patients during an 18-year period.
BMC Microbiol. 2012, 12, 155. [CrossRef] [PubMed]
100. Shah, A.A.; Hasan, F.; Ahmed, S.; Hameed, A. Characteristics, epidemiology and clinical importance of
emerging strains of Gram-negative bacilli producing extended-spectrum beta-lactamases. Res. Microbiol.
2004, 155, 409–421. [CrossRef] [PubMed]
101. Frost, L.S.; Leplae, R.; Summers, A.O.; Toussaint, A. Mobile genetic elements: The agents of open source
evolution. Nat. Rev. Microbiol. 2005, 3, 722–732. [CrossRef] [PubMed]
102. Malachowa, N.; DeLeo, F.R. Mobile genetic elements of Staphylococcus aureus. Cell. Mol. Life Sci. 2010,
67, 3057–3071. [CrossRef] [PubMed]
103. Allen, H.K.; Donato, J.; Wang, H.H.; Cloud-Hansen, K.A.; Davies, J.; Handelsman, J. Call of the wild:
Antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 2010, 8, 251–259. [CrossRef]
[PubMed]
104. Valentin, L.; Sharp, H.; Hille, K.; Seibt, U.; Fischer, J.; Pfeifer, Y.; Michael, G.B.; Nickel, S.; Schmiedel, J.;
Falgenhauer, L.; et al. Subgrouping of ESBL-producing Escherichia coli from animal and human sources: An
approach to quantify the distribution of ESBL types between different reservoirs. Int. J. Med. Microbiol. 2014,
304, 805–816. [CrossRef] [PubMed]
105. Nehring, S.; Albrecht, U. Biotop, Habitat, Mikrohabitat—Ein Diskussionsbeitrag zur Begriffsdefinition.
Lauterbonia 2000, 38, 75–84.
106. Lötzli, K. Ökosystem. In Handbuch zur Ökologie; Kuttler: Berlin, Germany, 1993; pp. 288–295. Available
online: https://www.zobodat.at/pdf/Lauterbornia_2000_38_0075-0084.pdf (accessed on 30 October 2018).
107. Broens, E.M. Livestock-Associated Methicillin Resistant Staphylococcus Aureus in Pigs—Prevalence, Risk Factors
and Transmission Dynamics; Wageningen University: Wageningen, The Netherlands, 2011.
108. Armand-Lefevre, L.; Ruimy, R.; Andremont, A. Clonal comparison of Staphylococcus aureus isolates from
healthy pig farmers, human controls, and pigs. Emerg. Infect. Dis. 2005, 11, 711–714. [CrossRef] [PubMed]
109. Graveland, H.; Wagenaar, J.A.; Bergs, K.; Heesterbeek, H.; Heederik, D. Persistence of livestock associated
MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE 2011, 6, e16830. [CrossRef]
[PubMed]
110. Lozano, C.; Aspiroz, C.; Charlez, L.; Gómez-Sanz, E.; Toledo, M.; Zarazaga, M.; Torres, C. Skin lesion by
methicillin-resistant Staphylococcus aureus ST398-t1451 in a Spanish pig farmer: Possible transmission from
animals to humans. Vector Borne Zoonotic Dis. 2011, 11, 605–607. [CrossRef] [PubMed]
111. Gilbert, M.J.; Bos, M.E.; Duim, B.; Urlings, B.A.; Heres, L.; Wagenaar, J.A.; Heederik, D.J. Livestock-associated
MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure.
Occup. Environ. Med. 2012, 69, 472–478. [CrossRef] [PubMed]
112. Agersø, Y.; Vigre, H.; Cavaco, L.M.; Josefsen, M.H. Comparison of air samples, nasal swabs, ear-skin swabs
and environmental dust samples for detection of methicillin-resistant Staphylococcus aureus (MRSA) in pig
herds. Epidemiol. Infect. 2014, 142, 1727–1736. [CrossRef] [PubMed]
113. Agersø, Y.; Aarestrup, F.M.; Pedersen, K.; Seyfarth, A.M.; Struve, T.; Hasman, H. Prevalence of
extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail
meat identified by selective enrichment and association with cephalosporin usage. J. Antimicrob. Chemother.
2012, 67, 582–588. [CrossRef] [PubMed]
114. Jakobsen, L.; Kurbasic, A.; Skjøt-Rasmussen, L.; Ejrnaes, K.; Porsbo, L.J.; Pedersen, K.; Jensen, L.B.;
Emborg, H.D.; Agersø, Y.; Olsen, K.E.; et al. Escherichia coli isolates from broiler chicken meat, broiler
chickens, pork, and pigs share phylogroups and antimicrobial resistance with community-dwelling humans
and patients with urinary tract infection. Foodborne Pathog. Dis. 2010, 7, 537–547. [CrossRef] [PubMed]

257
Sustainability 2018, 10, 3967

115. Guardabassi, L. Sixty years of antimicrobial use in animals: what is next? Vet. Rec. 2013, 173, 599–603.
[CrossRef] [PubMed]
116. Smet, A.; Martel, A.; Persoons, D.; Dewulf, J.; Heyndrickx, M.; Cloeckaert, A.; Praud, K.; Claeys, G.; Catry, B.;
Herman, L.; et al. Comparative analysis of extended-spectrum-β-lactamase-carrying plasmids from different
members of Enterobacteriaceae isolated from poultry, pigs and humans: Evidence for a shared β-lactam
resistance gene pool? J. Antimicrob. Chemother. 2009, 63, 1286–1288. [CrossRef] [PubMed]
117. Wulf, M.W.; Tiemersma, E.; Kluytmans, J.; Bogaers, D.; Leenders, A.C.; Jansen, M.W.; Berkhout, J.; Ruijters, E.;
Haverkate, D.; Isken, M.; et al. MRSA carriage in healthcare personnel in contact with farm animals.
J. Hosp. Infect. 2008, 70, 186–190. [CrossRef] [PubMed]
118. Vanderhaeghen, W.; Hermans, K.; Haesebrouck, F.; Butaye, P. Methicillin-resistant Staphylococcus aureus
(MRSA) in food production animals. Epidemiol. Infect. 2010, 138, 606–625. [CrossRef] [PubMed]
119. Köck, R.; Harlizius, J.; Bressan, N.; Laerberg, R.; Wieler, L.H.; Witte, W.; Deurenberg, R.H.; Voss, A.; Becker, K.;
Friedrich, A.W. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus
(MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur. J. Clin.
Microbiol. Infect. Dis. 2009, 28, 1375–1382. [CrossRef] [PubMed]
120. Kraemer, J.G.; Pires, J.; Kueffer, M.; Semaani, E.; Endimiani, A.; Hilty, M.; Oppliger, A. Prevalence of
extended-spectrum β-lactamase-producing Enterobacteriaceae and Methicillin-Resistant Staphylococcus
aureus in pig farms in Switzerland. Sci. Total Environ. 2017, 603–604, 401–405. [CrossRef] [PubMed]
121. Schouten, J.M.; Bouwknegt, M.; van de Giessen, A.W.; Frankena, K.; De Jong, M.C.; Graat, E.A. Prevalence
estimation and risk factors for Escherichia coli O157 on Dutch dairy farms. Prev. Vet. Med. 2004, 64, 49–61.
[CrossRef] [PubMed]
122. Correira-Gomes, C.; Economou, T.; Bailey, T.; Brazdil, P.; Vieira-Pinto, M.; Niza-Ribiero, J. Simulation Model
for Salmonella Typhimurium on a Farrow-to-Finish herd. In Proceedings of the 10th International Conference
on the Epidemiology and Control of Biological, Chemical and Physical Hazards in Pigs and Pork, Lisbon,
Portugal, 9–12 September 2013.
123. Grøntvedt, C.A.; Elstrøm, P.; Stegger, M.; Skov, R.L.; Skytt Andersen, P.; Larssen, K.W.; Urdahl, A.M.;
Angen, Ø.; Larsen, J.; Åmdal, S.; et al. Methicillin-Resistant Staphylococcus aureus CC398 in humans and
pigs in Norway: A “One Health” perspective on introduction and transmission. Clin. Infect. Dis. 2016,
63, 1431–1438. [CrossRef] [PubMed]
124. Cernicchiaro, N.; Pearl, D.L.; Ghimire, S.; Gyles, C.L.; Johnson, R.P.; LeJeune, J.T.; Ziebell, K.; McEwen, S.A.
Risk factors associated with Escherichia coli O157:H7 in Ontario beef cow-calf operations. Prev. Vet. Med.
2009, 92, 106–115. [CrossRef] [PubMed]
125. Snow, L.C.; Warner, R.G.; Cheney, T.; Wearing, H.; Stokes, M.; Harris, K.; Teale, C.J.; Coldham, N.G. Risk
factors associated with extended spectrum beta-lactamase Escherichia coli (CTX-M) on dairy farms in North
West England and North Wales. Prev. Vet. Med. 2012, 106, 225–234. [CrossRef] [PubMed]
126. Schmithausen, R.M.; Schulze-Geisthoevel, S.V.; Stemmer, F.; El-Jade, M.; Reif, M.; Hack, S.; Meilaender, A.;
Montabauer, G.; Fimmers, R.; Parcina, M.; et al. Analysis of transmission of MRSA and ESBL-E among pigs
and farm personnel. PLoS ONE 2015, 10, e0138173. [CrossRef] [PubMed]
127. Broens, E.M.; Graat, E.A.; Van der Wolf, P.J.; Van de Giessen, A.W.; De Jong, M.C. Prevalence and risk
factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Prev. Vet. Med. 2011,
102, 41–49. [CrossRef] [PubMed]
128. Schmithausen, R.M.; Kellner, S.R.; Schulze-Geisthoevel, S.V.; Hack, S.; Engelhart, S.; Bodenstein, I.;
Al-Sabti, N.; Reif, M.; Fimmers, R.; Körber-Irrgang, B.; et al. Eradication of methicillin-resistant
Staphylococcus aureus and of Enterobacteriaceae expressing extended-spectrum beta-lactamases on a
model pig farm. Appl. Environ. Microbiol. 2015, 81, 7633–7643. [CrossRef] [PubMed]
129. Mannion, C.; Leonard, F.C.; Lynch, P.B.; Egan, J. Efficacy of cleaning and disinfection on pig farms in Ireland.
Vet. Rec. 2007, 161, 371–375. [CrossRef] [PubMed]
130. Heinemann, C.; Steinhoff-Wagner, J.; Petersen, B. Evaluation of methods for determining cleaning
performances in pig stables. J. Anim. Sci. 2017, 95, 48. [CrossRef]
131. Wellington, E.M.; Boxall, A.B.; Cross, P.; Feil, E.J.; Gaze, W.H.; Hawkey, P.M.; Johnson-Rollings, A.S.;
Jones, D.L.; Lee, N.M.; Otten, W.; et al. The role of the natural environment in the emergence of antibiotic
resistance in gram-negative bacteria. Lancet Infect. Dis. 2013, 13, 155–165. [CrossRef]

258
Sustainability 2018, 10, 3967

132. Young, J.S.; Gormley, E.; Wellington, E.M. Molecular detection of Mycobacterium bovis and Mycobacterium
bovis BCG (Pasteur) in soil. Appl. Environ. Microbiol. 2005, 71, 1946–1952. [CrossRef] [PubMed]
133. Gaze, W.H.; Burroughs, N.; Gallagher, M.P.; Wellington, E.M. Interactions between Salmonella typhimurium
and Acanthamoeba polyphaga, and observation of a new mode of intracellular growth within contractile
vacuoles. Microb. Ecol. 2003, 46, 358–369. [CrossRef] [PubMed]
134. Beuchat, L.R. Ecological factors influencing survival and growth of human pathogens on raw fruits and
vegetables. Microbes Infect. 2002, 4, 413–423. [CrossRef]
135. Hiroi, M.; Harada, T.; Kawamori, F.; Takahashi, N.; Kanda, T.; Sugiyama, K.; Masuda, T.; Yoshikawa, Y.;
Ohashi, N. A survey of β-lactamase-producing Escherichia coli in farm animals and raw retail meat in
Shizuoka Prefecture, Japan. Jpn. J. Infect. Dis. 2011, 64, 153–155. [PubMed]
136. Blanc, V.; Mesa, R.; Saco, M.; Lavilla, S.; Prats, G.; Miró, E.; Navarro, F.; Cortés, P.; Llagostera, M. ESBL-
and plasmidic class C beta-lactamase-producing E. coli strains isolated from poultry, pig and rabbit farms.
Vet. Microbiol. 2006, 118, 299–304. [CrossRef] [PubMed]
137. Mesa, R.J.; Blanc, V.; Blanch, A.R.; Cortés, P.; González, J.J.; Lavilla, S.; Miró, E.; Muniesa, M.;
Saco, M.; Tórtola, M.T.; et al. Extended-spectrum beta-lactamase-producing Enterobacteriaceae in different
environments (humans, food, animal farms and sewage). J. Antimicrob. Chemother. 2006, 58, 211–215.
[CrossRef] [PubMed]
138. Heuer, H.; Schmitt, H.; Smalla, K. Antibiotic resistance gene spread due to manure application on agricultural
fields. Curr. Opin. Microbiol. 2011, 14, 236–243. [CrossRef] [PubMed]
139. Müller, W.; Wieser, P.; Woiwode, J. Zur Größe koloniebildender Einheiten in der Stallluft. Berl. Münch.
Tierärztl. Wschr. 1977, 90, 6–11.
140. Green, C.F.; Gibbs, S.G.; Tarwater, P.M.; Mota, L.C.; Scarpino, P.V. Bacterial plume emanating from the air
surrounding swine confinement operations. J. Occup. Environ. Hyg. 2006, 3, 9–15. [CrossRef] [PubMed]
141. Hartung, J.; Seedorf, J.; Trickl, T.; Gronauer, H. Emission of particulates from a pig farm with central air
exhaust in the pig stall. Deutsche Tierarztliche Wochenschrift 1998, 105, 244–245. [PubMed]
142. Zucker, B.A.; Trojan, S.; Müller, W. Airborne gram-negative bacterial flora in animal houses. J. Vet. Med. B
Infect. Dis. Vet. Public Health 2000, 47, 37–46. [CrossRef] [PubMed]
143. Künneken, J. Simulation der Tier-Bakterium-Umwelt-Interaktion im Biotop “Abferkelstall”; University of Bonn:
Bonn, Germany, 1991.
144. Hartung, J.; Whyte, R. Erfassung und Bewertung von Luftverunreinigungen in der Nutztierhaltung.
Atemwegs-Lungenkr. 1994, 20, 17–25.
145. Venglovský, J.; Gregová, G.; Kmet’, V.; Sasáková, N. Detection of airborne microorganisms and antibiotic
resistance from animal housing facilities. In Proceedings of the XVth International Congress of the
International Society for Animal Hygiene, Vienna, Austria, 12–16 August 2011; pp. 813–815.
146. Hilliger, H.G. Determination of bacterial flora in stall air. Zentralbl Veterinarmed B 1984, 31, 493–504. [CrossRef]
[PubMed]
147. Benbough, J.E. Death mechanisms in airborne Escherichia coli. J. Gen. Microbiol. 1967, 47, 325–333. [CrossRef]
[PubMed]
148. Gundermann, K.O. Life-span of bacterial strains in dust as influenced by various degrees of air humidity.
Zentralbl Bakteriol Orig B 1972, 156, 422–429. [PubMed]
149. Hoffmann, D.H. Experimental endogenous inflammation of the internal eye by Candida albicans.
Ophthalmoscopic, histological and microbiological studies on the course of the infection in rabbits.
Ophthalmologica 1966, 151, 1–84. [PubMed]
150. Weese, J.S.; DaCosta, T.; Button, L.; Goth, K.; Ethier, M.; Boehnke, K. Isolation of methicillin-resistant
Staphylococcus aureus from the environment in a veterinary teaching hospital. J. Vet. Intern. Med. 2004,
18, 468–470. [CrossRef] [PubMed]
151. Gibbs, S.G.; Green, C.F.; Tarwater, P.M.; Scarpino, P.V. Airborne antibiotic resistant and nonresistant bacteria
and fungi recovered from two swine herd confined animal feeding operations. J. Occup. Environ. Hyg. 2004,
1, 699–706. [CrossRef] [PubMed]
152. Bos, M.E.; Verstappen, K.M.; van Cleef, B.A.; Dohmen, W.; Dorado-García, A.; Graveland, H.; Duim, B.;
Wagenaar, J.A.; Kluytmans, J.A.; Heederik, D.J. Transmission through air as a possible route of exposure for
MRSA. J. Expo. Sci. Environ. Epidemiol. 2016, 26, 263–269. [CrossRef] [PubMed]

259
Sustainability 2018, 10, 3967

153. Heinemann, C.; Schmithausen, R.M.; Sib, E.; Meyer, I.; Petersen, B.; Steinhoff-Wagner, J. Preventive effect
of nasal lavage with physiologic saline on the colonization with MRSA after working in porcine stable.
J. Anim. Sci. 2017, 95, 250. [CrossRef]
154. Bos, M.E.; Taverne, F.J.; van Geijlswijk, I.M.; Mouton, J.W.; Mevius, D.J.; Heederik, D.J.; SDa, N.V.M.A.
Consumption of antimicrobials in pigs, veal calves, and broilers in the Netherlands: Quantitative results of
nationwide collection of data in 2011. PLoS ONE 2013, 8, e77525. [CrossRef] [PubMed]
155. Wenke, C.; Pospiech, J.; Reutter, T.; Altmann, B.; Truyen, U.; Speck, S. Impact of different supply air and
recirculating air filtration systems on stable climate, animal health, and performance of fattening pigs in a
commercial pig farm. PLoS ONE 2018, 13, e0194641. [CrossRef] [PubMed]
156. Laube, H.; Friese, A.; von Salviati, C.; Guerra, B.; Rösler, U. Transmission of ESBL/AmpC-producing
Escherichia coli from broiler chicken farms to surrounding areas. Vet. Microbiol. 2014, 172, 519–527.
[CrossRef] [PubMed]
157. Von Salviati, C.; Laube, H.; Guerra, B.; Roesler, U.; Friese, A. Emission of ESBL/AmpC-producing Escherichia
coli from pig fattening farms to surrounding areas. Vet. Microbiol. 2015, 175, 77–84. [CrossRef] [PubMed]
158. Dohmen, W.; Schmitt, H.; Bonten, M.; Heederik, D. Air exposure as a possible route for ESBL in pig farmers.
Environ. Res. 2017, 155, 359–364. [CrossRef] [PubMed]
159. Laube, H.; Friese, A.; von Salviati, C.; Guerra, B.; Käsbohrer, A.; Kreienbrock, L.; Roesler, U. Longitudinal
monitoring of extended-spectrum-beta-lactamase/AmpC-producing Escherichia coli at German broiler
chicken fattening farms. Appl. Environ. Microbiol. 2013, 79, 4815–4820. [CrossRef] [PubMed]
160. Hoffmann, A. Presence of CTX-M-1 Group Extended-Spectrum-ß-Lactamase in Dust from Dutch Pig Farms; Utrecht
University: Utrecht, The Netherlands, 2014.
161. Lupo, A.; Coyne, S.; Berendonk, T.U. Origin and evolution of antibiotic resistance: The common mechanisms
of emergence and spread in water bodies. Front. Microbiol. 2012, 3, 18. [CrossRef] [PubMed]
162. Baquero, F.; Martínez, J.L.; Cantón, R. Antibiotics and antibiotic resistance in water environments. Curr.
Opin. Biotechnol. 2008, 19, 260–265. [CrossRef] [PubMed]
163. Coleman, B.L.; Salvadori, M.I.; McGeer, A.J.; Sibley, K.A.; Neumann, N.F.; Bondy, S.J.; Gutmanis, I.A.;
McEwen, S.A.; Lavoie, M.; Strong, D.; et al. The role of drinking water in the transmission of
antimicrobial-resistant E. coli. Epidemiol. Infect. 2012, 140, 633–642. [CrossRef] [PubMed]
164. Schwartz, T.; Kohnen, W.; Jansen, B.; Obst, U. Detection of antibiotic-resistant bacteria and their resistance
genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol. Ecol. 2003, 43, 325–335.
[CrossRef] [PubMed]
165. Mulamattathil, S.G.; Esterhuysen, H.A.; Pretorius, P.J. Antibiotic-resistant gram-negative bacteria in a
virtually closed water reticulation system. J. Appl. Microbiol. 2000, 88, 930–937. [PubMed]
166. Kaspar, C.W.; Burgess, J.L.; Knight, I.T.; Colwell, R.R. Antibiotic resistance indexing of Escherichia coli to
identify sources of fecal contamination in water. Can. J. Microbiol. 1990, 36, 891–894. [CrossRef] [PubMed]
167. Ozgumus, O.B.; Celik-Sevim, E.; Alpay-Karaoglu, S.; Sandalli, C.; Sevim, A. Molecular characterization of
antibiotic resistant Escherichia coli strains isolated from tap and spring waters in a coastal region in Turkey.
J. Microbiol. 2007, 45, 379–387. [PubMed]
168. Gao, P.; Munir, M.; Xagoraraki, I. Correlation of tetracycline and sulfonamide antibiotics with corresponding
resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant.
Sci. Total Environ. 2012, 421–422, 173–183. [CrossRef] [PubMed]
169. Madec, J.Y.; Haenni, M.; Ponsin, C.; Kieffer, N.; Rion, E.; Gassilloud, B. Sequence Type 48 Escherichia coli
Carrying the blaCTX-M-1 IncI1/ST3 Plasmid in Drinking Water in France. Antimicrob. Agents Chemother.
2016, 60, 6430–6432. [CrossRef] [PubMed]
170. Zarfel, G.; Lipp, M.; Gürtl, E.; Folli, B.; Baumert, R.; Kittinger, C. Troubled water under the bridge: Screening
of River Mur water reveals dominance of CTX-M harboring Escherichia coli and for the first time an
environmental VIM-1 producer in Austria. Sci. Total Environ. 2017, 593–594, 399–405. [CrossRef] [PubMed]
171. Kittinger, C.; Lipp, M.; Baumert, R.; Folli, B.; Koraimann, G.; Toplitsch, D.; Liebmann, A.; Grisold, A.J.;
Farnleitner, A.H.; Kirschner, A.; et al. Antibiotic resistance patterns of pseudomonas spp. isolated from the
River Danube. Front. Microbiol. 2016, 7, 586. [CrossRef] [PubMed]
172. LeJeune, J.T.; Besser, T.E.; Merrill, N.L.; Rice, D.H.; Hancock, D.D. Livestock drinking water microbiology
and the factors influencing the quality of drinking water offered to cattle. J. Dairy Sci. 2001, 84, 1856–1862.
[CrossRef]

260
Sustainability 2018, 10, 3967

173. LeJeune, J.T.; Besser, T.E.; Hancock, D.D. Cattle water troughs as reservoirs of Escherichia coli O157.
Appl. Environ. Microbiol. 2001, 67, 3053–3057. [CrossRef] [PubMed]
174. Pletinckx, L.J.; Verhegghe, M.; Dewulf, J.; Crombé, F.; De Bleecker, Y.; Rasschaert, G.; Goddeeris, B.M.;
De Man, I. Screening of poultry-pig farms for methicillin-resistant Staphylococcus aureus: Sampling
methodology and within herd prevalence in broiler flocks and pigs. Infect. Genet. Evol. 2011, 11, 2133–2137.
[CrossRef] [PubMed]
175. Porrero, M.C.; Mentaberre, G.; Sánchez, S.; Fernández-Llario, P.; Casas-Díaz, E.; Mateos, A.; Vidal, D.;
Lavín, S.; Fernández-Garayzábal, J.F.; Domínguez, L. Carriage of Staphylococcus aureus in free-living wild
animals in Spain. Appl. Environ. Microbiol. 2014. [CrossRef] [PubMed]
176. van der Wolf, P.J.; Rothkamp, A.; Junker, K.; de Neeling, A.J. Staphylococcus aureus (MSSA) and MRSA
(CC398) isolated from post-mortem samples from pigs. Vet. Microbiol. 2012, 158, 136–141. [CrossRef]
[PubMed]
177. Exner, M.; Kramer, A.; Lajoie, L.; Gebel, J.; Engelhart, S.; Hartemann, P. Prevention and control of health
care-associated waterborne infections in health care facilities. Am. J. Infect. Control 2005, 33, S26–S40.
[CrossRef] [PubMed]
178. Hartung, J. Rules to control drinking water supply systems in livestock farming. Deutsche Tierarztliche Wochenschrift
2000, 107, 302–304. [PubMed]
179. Hartung, J.; Kamphues, J. Do we need regulation of drinking water for animals? Recommendations for the
water supply of farm animals and pets. Deutsche Tierarztliche Wochenschrift 2000, 107, 343–345. [PubMed]
180. Jutkina, J.; Marathe, N.P.; Flach, C.F.; Larsson, D.G.J. Antibiotics and common antibacterial biocides stimulate
horizontal transfer of resistance at low concentrations. Sci. Total Environ. 2018, 616–617, 172–178. [CrossRef]
[PubMed]
181. Hölzel, C.S.; Schwaiger, K.; Harms, K.; Küchenhoff, H.; Kunz, A.; Meyer, K.; Müller, C.; Bauer, J. Sewage
sludge and liquid pig manure as possible sources of antibiotic resistant bacteria. Environ. Res. 2010,
110, 318–326. [CrossRef] [PubMed]
182. Ben Said, L.; Jouini, A.; Klibi, N.; Dziri, R.; Alonso, C.A.; Boudabous, A.; Ben Slama, K.; Torres, C. Detection
of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of
the farm environment in Tunisia. Int. J. Food Microbiol. 2015, 203, 86–92. [CrossRef] [PubMed]
183. Purohit, M.R.; Chandran, S.; Shah, H.; Diwan, V.; Tamhankar, A.J.; Stålsby Lundborg, C. Antibiotic resistance
in an Indian rural community: A ‘One-Health’ observational study on commensal coliform from humans,
animals, and water. Int. J. Environ. Res. Public Health 2017, 14, 386. [CrossRef] [PubMed]
184. Vital, P.G.; Zara, E.S.; Paraoan, C.E.M.; Dimasupil, A.Z.; Abello, J.J.M.; Santos, I.T.G.; Rivera, W.L. Antibiotic
resistance and extended-spectrum Beta-Lactamase production of Escherichia coli isolated from irrigation
waters in selected urban farms in metro Manila, Philippines. Water 2018, 10, 548. [CrossRef]
185. Zurfluh, K.; Power, K.A.; Klumpp, J.; Wang, J.; Fanning, S.; Stephan, R. A novel Tn3-like composite
transposon harboring blaVIM-1 in Klebsiella pneumoniae spp. pneumoniae isolated from river water.
Microb. Drug Resist. 2015, 21, 43–49. [CrossRef] [PubMed]
186. Moore, J.E.; Watabe, M.; Millar, B.C.; Loughrey, A.; McCalmont, M.; Goldsmith, C.E.; Heaney, J.C.; Buckley, T.;
Egan, C.; McDowell, D.A.; et al. Screening of clinical, food, water and animal isolates of Escherichia coli
for the presence of blaCTX-M extended spectrum beta-lactamase (ESBL) antibiotic resistance gene loci.
Ulster Med. J. 2010, 79, 85–88. [PubMed]
187. Ikegbunam, M.N.; Anagu, L.O.; Iroha, I.R.; Ejikeugwu, C.E.; Esimone, C.O. Abattoirs as non-hospital
source of extended spectrum beta lactamase producers: Confirmed by the double disc synergy test and
characterized by matrix-assisted laser desorption/ionization time of flight mass spectrometry. PLoS ONE
2014, 9, e94461. [CrossRef] [PubMed]
188. Johnson, J.R.; Sannes, M.R.; Croy, C.; Johnston, B.; Clabots, C.; Kuskowski, M.A.; Bender, J.; Smith, K.E.;
Winokur, P.L.; Belongia, E.A. Antimicrobial drug-resistant Escherichia coli from humans and poultry
products, Minnesota and Wisconsin, 2002–2004. Emerg. Infect. Dis. 2007, 13, 838–846. [CrossRef] [PubMed]
189. Vincent, C.; Boerlin, P.; Daignault, D.; Dozois, C.M.; Dutil, L.; Galanakis, C.; Reid-Smith, R.J.; Tellier, P.P.;
Tellis, P.A.; Ziebell, K.; et al. Food reservoir for Escherichia coli causing urinary tract infections.
Emerg. Infect. Dis. 2010, 16, 88–95. [CrossRef] [PubMed]

261
Sustainability 2018, 10, 3967

190. Lavilla, S.; González-López, J.J.; Miró, E.; Domínguez, A.; Llagostera, M.; Bartolomé, R.M.;
Mirelis, B.; Navarro, F.; Prats, G. Dissemination of extended-spectrum beta-lactamase-producing bacteria:
The food-borne outbreak lesson. J. Antimicrob. Chemother. 2008, 61, 1244–1251. [CrossRef] [PubMed]
191. Normanno, G.; Dambrosio, A.; Lorusso, V.; Samoilis, G.; Di Taranto, P.; Parisi, A. Methicillin-resistant
Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy. Food Microbiol. 2015,
51, 51–56. [CrossRef] [PubMed]
192. Sommer, M. Epidemiologische Untersuchungen zur Tiergesundheit in Schweinezuchtbeständen unter
besonderer Berücksichtigung von Managementfaktoren und des Einsatzes von Antibiotika und Homöopathika;
Hanover University: Hanover, Germany, 2009.
193. Walker, B.; Holling, C.S.; Carpenter, S.; Kinzig, A. Resilience, adaptability and transformability in
social-ecological systems. Ecol. Soc. 2004, 5, 9. [CrossRef]
194. Rauw, W.M.; Kanis, E.; Noordhuizen-Stassen, E.N.; Grommers, F.J. Undesirable side effects of selection for
high production efficiency in farm animals: A review. Livest. Prod. Sci. 1998, 56, 15–33. [CrossRef]
195. Tenhagen, B.-A.; Fetsch, A.; Alt, K.; Käsbohrer, A.; Bräunig, A.; Appel, B. MRSA in herds of fattening
pigs in Germany—Associated risk factors. In Proceedings of the Safe Pork 2009, Québec, QC, Canada,
30 September–2 October 2009.
196. Thielen, T.L.; Castle, S.S.; Terry, J.E. Anterior ocular infections: An overview of pathophysiology and
treatment. Ann. Pharmacother. 2000, 34, 235–246. [CrossRef] [PubMed]
197. Steinhoff-Wagner, J. Ethische Zielkonflikte aus agrarwissenschaftlicher Perspektive. 2018; unpublished data.
198. Hörügel, K. Tiergesundheitsmanagement in der Schweinehaltung. Schriftenreihe der Sächsischen Landesanstalt
für Landwirtschaft 2001, 7, 63–67.
199. Böckel, V. Untersuchungen zur quantitativen Bewertung der Tiergesundheit von Schweinebeständen; Hanover
University: Hanover, Germany, 2008.
200. Berns, G. Einbindung von Check-Listen und mobilen Analyselabor in Beratungskonzepte zur Erweiterung von
Gesundheitsvorsorge- und Qualitätsmanagementsystemen in der Schweinefleischerzeugung; University of Bonn:
Bonn, Germany, 1996.
201. Düsseldorf, S. Concept of key Performance Indicators Controlling Consumer Oriented Quality and Herd Health
Management in a Bavarian Pork Chain; Univertiy of Bonn: Bonn, Germany, 2013.
202. Ellebrecht, A. Nutzenbetrachtung Internetbasierter Informationssysteme im Einzel- und Überbetrieblichen
Gesundheitsmanagement; University of Bonn: Bonn, Germany, 2008.
203. Ellebrecht, S. Application Concept for Combined Preventive Quality Management methods in inter-Enterprise Health
Management in Pork Chains; University of Bonn: Bonn, Germany, 2012.
204. Gymnich, S. Haptoglobin als Screeningparameter im Gesundheitsmanagement von Ferkelaufzuchtbetrieben;
University of Bonn: Bonn, Germany, 2001.
205. Klauke, T. Risk Based Approach towards More Sustainablilty in European Pig Production; University of Bonn:
Bonn, Germany, 2012.
206. Mack, A. Konzeption für Die Anwendung Computergestützter Techniken im Gesundheitsmanagement
Fleischerzeugender Ketten; University of Bonn: Bonn, Germany, 2009.
207. Schütz, V. Modell zur Planung von Dienstleistungen für das Überbetriebliche Gesundheitsmanagement in der
Fleischwirtschaft; University of Bonn: Bonn, Germany, 2009.
208. Welz, M. Bewertung von Erkrankungen als Qualitätshemmende Faktoren mit Hilfe der Fehler- Möglichkeits- und
Einfluss-Analyse (FMEA) im Rahmen der Erzeugung von Qualitätsfleisch; Bonn University: Bonn, Germany, 1993.
209. Schulze Althoff, G. Konzept und Erprobung von Werkzeugen für Grenzüberschreitende, Kettenübergreifende
Qualitätsmanagementsysteme in der Schweinefleischerzeugung; University of Bonn: Bonn, Germany, 2007.
210. Petersen, B.; Nüssel, M.; Hamer, M. Quality and risk management in agri-food chains. In European Review of
Agricultural Economics; Wageningen Academic Publishers: Wageningen, The Netherlands, 2014; pp. 1–3.
211. Schulze Althoff, G.; Breuer, O.; Jaeger, F.; Petersen, B. Working together to improve early warning—Cross
border approaches to advancing prevention concepts. Fleischwirtsch. Int. 2007, 2, 55–58.
212. Petersen, J.V.; Andersen, J.K.; Sørensen, F.; Knudsen, H. Food safety on the slaughterline: Inspection of pig
heads. Vet. Rec. 2002, 150, 782–784. [CrossRef] [PubMed]
213. Petersen, B.; Spiller, A.; Theuvsen, L. Vom Viehmarkter zum Dienstleistungsprofi; GIQS: Bonn, Germany, 2010.
214. Lehnert, H. Animal health monitoring. TopAgrar 2009, 11, 12–17.

262
Sustainability 2018, 10, 3967

215. Schiefer, G. Tracking, Tracing and Business Process Interests: A Framework for Analysis. In Proceedings
of the 26th Conference of the International Association of Agricultural Economists, Queensland, Australia,
12–16 August 2006.
216. Van der Vorst, J. Effective Food Supply Chains. Generating, Modelling and Evaluating Supply Chain Scenarios;
University Wageningen: Wageningen, The Netherlands, 2000.
217. Petersen, B.; Lehnert, S. Qualitätsmanagement Maßgeschneidert für die Agrar- und Ernährungswirtschaft; Rheinische
Friedrich-Wilhelms-Universität Bonn, International FoodNetCenter: Bonn, Germany, 2017; Volume 1.
218. Ewers, C.; Bethe, A.; Semmler, T.; Guenther, S.; Wieler, L.H. Extended-spectrum β-lactamase-producing and
AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on
public health: A global perspective. Clin. Microbiol. Infect. 2012, 18, 646–655. [CrossRef] [PubMed]
219. Ferreira, J.P.; Anderson, K.L.; Correa, M.T.; Lyman, R.; Ruffin, F.; Reller, L.B.; Fowler, V.G. Transmission of
MRSA between companion animals and infected human patients presenting to outpatient medical care
facilities. PLoS ONE 2011, 6, e26978. [CrossRef] [PubMed]
220. Häsler, B. (NEOH) Network for Evaluation of One Health. Available online: http://www.accelopment.com/
de/projects/neoh (accessed on 23 October 2018).
221. Steinhoff-Wagner, J.; Ilg, Y.; Tappe, E.-V.; Lehnert, S.; Lehnert, H.; Petersen, B. One Health-Konzepte und ihre
Umsetzung—Forschungsprojekte, Hochschulausbildung und Netzwerkinitiativen; ATD: Bonn, Germany, 2017; Volume 2.
222. De Neeling, A.J.; van den Broek, M.J.; Spalburg, E.C.; van Santen-Verheuvel, M.G.; Dam-Deisz, W.D.;
Boshuizen, H.C.; van de Giessen, A.W.; van Duijkeren, E.; Huijsdens, X.W. High prevalence of methicillin
resistant Staphylococcus aureus in pigs. Vet. Microbiol. 2007, 122, 366–372. [CrossRef] [PubMed]
223. Dickhöfer, D. Haptoglobin als Screeningparameter für Atemwegserkrankungen des Schweines; University of Bonn
and University of Veterinary Medicine Hannover: Hannover, Germany, 2002.
224. Lipperheide, C.; Knura, S.; Petersen, B. Sicherung der Regionalen Vermarktung von Ferkeln für
Nordrhein-Westfälische Qualitätsfleischprogramme Durch die Einführung Überbetrieblicher Gesundheitsmanagement-
und Frühwarnsysteme; Lehr- und Forschungsschwerpunkt “Umweltverträgliche und Standortgerechte
Landwirtschaft”: Bonn, Germany, 1999.
225. BMEL. 16. AMG-Novelle des Arzneimittelgesetzes; BMELV: Bonn, Germany, 2014.
226. QS. Wenn es um Fleisch geht. Qualität. Warenkunde. Küchentechniken. Rezeptideen. In Qualitätssicherung.
Vom Landwirt bis zur Ladentheke; QS: Bonn, Germany, 2011; Available online: https://www.q-s.de/flip/
ratgeber_fleisch/files/assets/downloads/publication.pdf (accessed on 23 October 2018).
227. Merle, R.; Kösters, S.; May, T.; Portsch, U.; Blaha, T.; Kreienbrock, L. Serological Salmonella monitoring in
German pig herds: Results of the years 2003–2008. Prev. Vet. Med. 2011, 99, 229–233. [CrossRef] [PubMed]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

263
 sustainability

Article
The Valorization of Ammonia in Manure Digestate by
Means of Alternative Stripping Reactors
Marco Baldi 1, *, Maria Cristina Collivignarelli 2 ID
, Alessandro Abbà 3 ID
and Ilaria Benigna 2
1 Department of Chemistry, University of Pavia, viale Taramelli 10, 27100 Pavia, Italy
2 Department of Civil Engineering and Architecture, University of Pavia, via Ferrata 1, 27100 Pavia, Italy;
[email protected] (M.C.C.); [email protected] (I.B.)
3 Department of Civil, Environmental, Architectural Engineering and Mathematics, University of Brescia,
via Branze 43, 25123 Brescia, Italy; [email protected]
* Correspondence: [email protected]; Tel.: +39-03-8298-7270

Received: 12 July 2018; Accepted: 27 August 2018; Published: 29 August 2018

Abstract: The proper recovery of resources such as nitrogen and phosphorus present in the manure
from intensive livestock farming is essential in order to allow environmental sustainable zootechny
especially in densely populated areas where these activities are historically prevalent. The experiences
at full-scale established that the ammonia stripping allows recovery from 35% to 50% of nitrogen
depending on the type of substrate treated with anaerobic digestion and on the nitrogen content/form
in the digestate. This study focuses on the ammonia stripping on digestate derived from anaerobic
digestion of livestock manure and corn silage. Two different full-scale plants are studied including
a packed column and an air bubble reactor without filling material with the aim to reduce fouling
issues due to the content of suspended solids in digestate. The main results suggest that the use of an
air bubble reactor could treat digestate with high concentration of suspended solids. A deeper study
based on a two-level factorial experiment highlights that the temperature is an important parameter
that influences the ammonia removal yields. Thus, a proper management of available thermal energy
is very important.

Keywords: anaerobic digestion; livestock manure; digestate; ammonia recovery; fouling issue

1. Introduction
The management of agricultural waste, animal manure (bovine, swine, and poultry), and food
residues by means of anaerobic digestion (AD) is becoming more important [1,2]. In anaerobic
digestion (AD), the microorganisms in the absence of oxygen break down the biodegradable matter
and produce a valuable biogas consisting of mostly methane [3]. The biogas can either be used directly
or it can be converted into electrical energy. The other residue of anaerobic digestion is digestate [4].
The digestate represents the AD effluent (i.e., the digested substrate), which is removed from the reactor.
The nature and composition of treated substrate and the operating parameters of the AD process have
a significant influence on the physical and chemical characteristics of digestate [3]. The ammonia
content of digestate depends on the total nitrogen content of feedstock. Cereal grains, poultry, and pig
manures show high ammonia content. However, the bovine manure and corn silage present a lower
ammonia content [5].
The main issues concerning the landspreading of digestate on agricultural soils that represents
the main route are related to the high content of nutrients especially nitrogen [6] and represent the
increasing number of AD plants especially in the region with intensive livestock farming [7]. Therefore,
in order to comply with the European Nitrates Directive (91/676/EEC) [8], suitable treatments for
nitrogen reduction in digestate must be applied. Moreover, the recent Italian legislation has restricted
the landspreading of digestate derived from AD of different materials and/or residues [9].

Sustainability 2018, 10, 3073; doi:10.3390/su10093073 264 www.mdpi.com/journal/sustainability

Sustainability 2018, 10, 3073

The first step of digestate treatments usually carried out at farm scale concerns the solid/liquid
separation. The solid fraction with high content of organic nitrogen can be spread on agricultural soils
directly or after a composting process [10]. In the liquid phase, the high contents of nitrogen generally
with high ammonia percentage, phosphorus, and other macro and micronutrients [11] represent a
serious problem for its recovery/disposal.
Furthermore, some authors [12] have studied the feasibility to increase the methane productions in
AD up to 104% [13] by using the pretreatment of animal manure fibers with aqueous ammonia soaking.
Despite this treatment being very interesting, the proposed solution could increase the ammonia
content in digestate involving, especially in Italy, additional issues for its recovery on agricultural soils.
As concerns grow regarding the ammonia removal from liquid digestate, several treatments
are proposed in the scientific literature. The methods based on physical-chemical processes include
struvite precipitation: the ammonia removal yields from the digestate of poultry manure reached 86.4%
(with Mg:N:P molar ratio of 1:1:1) and 97.4% (adjusting Mg:N:P molar ratio to 1.5:1:1) [14]. However,
the contents of heavy metals precipitated together with struvite [15] must be controlled.
The ammonia stripping on livestock manure digestates allowed to obtain ammonia removal
yields up to 85%, which operates at 40 ◦ C with a pH adjustment [16]. However, Serna-Maza et al. [17]
showed that the ammonia removal from fresh digestate was more difficult than digestate stored for
long periods.
Moreover, the evaporation is an interesting solution to remove nitrogen from pig slurry with a
previous anaerobic digestion to increase the economic feasibility [18]. Guercini et al. [19] proposed to
use the cogeneration heat to support both the AD plant and the subsequent evaporation of the digestate.
The membrane technology for ammonia removal from digestate could be applied. The use
of hollow fiber membranes, submerged into the digestate from the anaerobic reactor that treats
slaughterhouse wastes, led to a reduction of free ammonia by 70% [20]. However, the membrane
parameters (such as bubble point, breakthrough pressure, airflow, pore size, contact angle, thickness,
etc.) must be evaluated to predict the performance process [21]. As concerns the membrane processes,
an innovative solution based on a thermophilic aerobic membrane reactor for the treatment of
sewage sludge and high strength aqueous waste [22] is able to increase the ammonia content in
permeate and the precipitation of nutrients (nitrogen and phosphorus) in the form of salts. Moreover,
the proposed solution can be conveniently integrated in traditional wastewater treatment plants (based
on a conventional activated sludge process) with the aim to reduce the content of nutrients in the
discharged effluent and to recover the heat from the thermophilic aerobic reactor [23].
The choice of suitable technology and the required pretreatments depend on different aspects
mainly related to the qualitative characteristics of digestate. The ammonia stripping and chemical
precipitation require simple pretreatments (usually screw press or belt filter press) in order to reduce
the content of suspended solid. The other proposed technologies instead require pretreatments with
ultrafiltration (UF) followed by cleaning/regeneration cycles [24]. The farmers prefer to adopt simple
and robust treatment plants with low investment and maintenance costs.
The ammonia stripping technology is a process where the nitrogen, in the form of ammonia, is
removed from a liquid by gas flow through the liquid. The volatility of ammonia in an aqueous solution
can be enhanced by increasing the temperature and pH (usually obtained through chemical addition).
The ammonia stripping process includes the following operations [25]: (i) conversion of
ammonium ions (NH4 + ) to ammonia gas (NH3 ) (ammonia dissociation equilibrium), (ii) diffusion of
NH3 to the air-water interface (water-side mass transfer), (iii) release of NH3 to the air at the interface
(volatilization), and (iv) diffusion of NH3 from the air-water interface into the air above (air-side mass
transfer). The whole process depends on pH, temperature, and mass transfer area.
Ammonia gas (NH3 ) is thereafter absorbed in an acid solution (sulphuric or nitric acid) in order
to obtain fertilizer for agricultural use (ammonium sulphate or nitrate respectively) with low organic
contamination. The cleaned gas can be reused in the stripping column.

265
Sustainability 2018, 10, 3073

The efficiency of air stripping mainly depends on the following parameters: feed pH, feed
temperature, ratio of air to feed, and feed characteristics.
The high thermal energy requirement has often restricted the applicability of ammonia stripping.
Therefore, this technology is used when there is heat available, which results from the production of
electrical power by endothermic motors in excess of the intrinsic needs arising from the need to control
the temperature of the plant for the biogas production.
Concerning the stripping reactor, the design of the contacting system between the digestate and
the gas used to strip out the NH3 is very important. The aim is to maximize the extent of contact
(maximum rate of mixing and highest specific surface area) while minimizing energy costs due to
the equipment design. The most common mass transfer design for air stripping systems uses packed
towers: columns filled with packing material in order to increase the surface area available for the
ammonia mass transfer.
Despite the fact that most common reactors used for ammonia stripping are based on packed
columns, the suspended solids can clog the column. This aspect is called fouling. The high content
of suspended solids reduces the stripping performance. This reduction is due both to the fouling
that involves problems on stripping management and to high content of organic acids and colloidal
compounds that reduce the process efficiency [26]. As a consequence, efficient solid–liquid separation
is necessary beforehand. In addition, a high maintenance and cleaning effort may be necessary.
Regarding the nitrogen partition in livestock manure, Fabbri and Piccinini (2012) [27] show that,
in swine, manure ammonia represents about 60% of total nitrogen, which increases by 10% due to AD.
Even in the case of bovine manure, the AD involves an increase of ammonia content from 43% to 52%.
Furthermore, concerning the solid/liquid separation process, they show that the ammonia nitrogen
with respect to total nitrogen increases: (i) in the case of swine manure, from 70% to 90% and (ii) in the
case of bovine manure, from 50% to 70%.
In the present study, the ammonia recovery from digestate derived from the AD of swine, bovine,
poultry manure, and corn silage was analyzed. Experimental activities were carried out on two
different air stripping full-scale plants: the first is a packed column reactor and the second is an air
bubble reactor without filling material in order to reduce the issues concerning fouling. In this study,
the advantages and disadvantages of the alternative solutions are reported.

2. Material and Methods

In this section, the characteristics of the ammonia stripping plants at full-scale are reported.
The main characteristics of liquid digestate (treated in these plants) are also shown. Moreover, the
operative conditions of the tests carried out during the experimental activities are reported.

2.1. Description of Plants and Digestate Characteristics

The Figure 1 reports a schematic diagram of the process for the anaerobic treatment of livestock
manure and agricultural residues in order to recover ammonia as fertilizer. The treatment consists
of an anaerobic digestion where bovine, swine, poultry manure, and corn silage are fed as well as a
solid/liquid separation for the obtaining of liquid digestate and the subsequent ammonia recovery
section. Three different flows come from the treatment including: (i) the solid fraction, which is sent
to a composting process, (ii) the liquid fraction, which is sent to ammonia stripping, and (iii) the air
contaminated by ammonia, which is sent to an absorption tower for fertilizer production.

266
Sustainability 2018, 10, 3073

Figure 1. Schematic diagram of the process.

During the experimental activities, two different kinds of plants were used. The stripping reactor
of plant #1 consists of a packed column that receives the liquid digestate obtained from a rotary drum
with a mesh of 350 μm followed in a second phase of experimentation by a vibrating screen with a
mesh of 150 μm. The ammonia stripping section of plant #2 is an air bubble reactor that treats the
liquid digestate derived from a screw press separator with a mesh of 5 mm. Both plants are equipped
with a similar packing absorption tower for ammonium sulphate production (see Table 1).

Table 1. Geometrical characteristic of the plants.

Plant Section Parameter Plant #1 Plant #2

Diameter [m] 1.2 2.8
Surface [m2 ] 1.1 6
Packed height [m] 3 -
Ammonia stripping Liquid height [m] - 2
Specific surface of packing material [m2 m−3 ] 200 -
Recirculation flowrate [m3 h−1 ] 16 22
Air flowrate [Nm3 h−1 ] 4000–4500 500–700
Diameter [m] 0.8 0.55
Packed height [m] 3.0 2.5
Absorption tower Specific surface of packing material [m2 m−3 ] 245 245
H2 SO4 H2 SO4
Absorbent
(50% v/v solution) (50% v/v solution)

Regarding plant #1 (Figure 2a), the ammonia stripping reactor is a vertical column filled with
packing material. The specific surface is 200 m2 m−3 . The flow treated is 2.5 m3 h−1 and the air
flowrate is about 4500 m3 h−1 . In the first part of the experiment, plant #1 operated continuously
while, in a second period in a semi-batch mode (i.e., liquid phase in batch with air flow). In semi-batch
conditions, the volume of liquid digestate (5 m3 and 13.2 m3 for plant#1 and #2, respectively) was
maintained into the stripping reactor for a suitable time (2 h for plant #1 and 6 h for plant #2). The air
flowrate is supplied continuously.
In the stripping column of plant #2 (Figure 2b), the air is supplied with medium/fine bubble
diffusers. The plant worked both in continuous (with complete mixing) and in a semi-batch mode.
In both plants, the ammonia recovery is obtained in an acid scrubber with a pH of 4.3. In these
conditions, even if the concentration of ammonia in the absorbent solution reaches the 10% w/w
(weight to weight), the concentration of NH3 in the flu-gas is maintained around 3 to 5 mgN m−3 of
dry air. For the absorption process, a 50% v/v (volume/volume) sulphuric acid (H2 SO4 ) solution is
used, which allows the production of di-ammonium sulphate solution with a nitrogen content of 8%
to 10%.

267
Sustainability 2018, 10, 3073

The geometrical characteristics of the plants used in the experimental activities are reported in
Table 1. In Table 2, the qualitative characteristics of the liquid fraction of digestate fed to the different
plants are shown. It can be observed that plant #2 is able to treat liquid fraction with suspended solids
content up to 5%. This value cannot be reached in the case of plant #1 due to the issue concerning the
fouling of packing material. In fact, the configuration of plant #1 does not allow the treatment of the
substrate with a suspended solid content higher than 2%.

Figure 2. Ammonia recovery sections of plant #1 (a) and plant #2 (b).

Table 2. Qualitative characteristics of liquid digestate.

Parameter Plant #1 Plant #2

pH 7.7–8.2 7.7–8.2
Suspended solids [%] <2 2–5
Dissolved solids [%] 0.8–1.2 0.8–1.2
Ammoniacal nitrogen [g L−1 ] 2.5–3.5 2.0–3.0

2.2. Operative Conditions of Experimental Tests

The operative conditions of the tests carried out during the experiment are shown in Table 3.
Concerning plant #1, at the beginning of the experiment, it worked in a continuous mode (phase I)
with pH and temperature ranging from 9.5 to 10 pH and from 35 to 40 ◦ C, respectively. Then the plant
worked in semi-batch conditions (phase II) with pH ranges from 9.2 to 9.5. In this case, the alkaline
reagent (NaOH) consumption was significantly lower than in phase I.
The semi-batch conditions, due to the high rates of ammonia removal, reached the same
performance obtained in the continuous mode, but with pH values significantly lower, which indicates
an important reduction of alkaline reagent consumption.
The vibrating screen with a mesh of 150 μm works at the end of phase I.
At the beginning of experimental activities with plant #2, a preliminary test was performed in
semi-batch conditions using an aqueous solution of ammonium sulphate with ammonia concentration
equal to 2500 mgN L−1 . Then plant #2 worked in a continuous mode with a temperature of 48 ◦ C
and pH ranging from 9.5 to 10.1 (obtained with NaOH dosage). This test showed a foaming issue due
to the dosage of an alkaline reagent and the air supply with medium/fine bubble diffusers. Thus, 6
additional tests, always in a continuous mode, were performed without the use of an alkaline reagent
(4 tests) and with the presence of NaOH and a defoamer agent (2 tests).

268
Sustainability 2018, 10, 3073

Table 3. Operative conditions of experimental tests on plant #1 and #2.

Work Digestate Flowrate Temperature Air Flowrate

Plant Day Test # HRT [h] pH
Condition [m3 h−1 ] [◦ C] [Nm3 h−1 ]
0 1 38.5 9.5
24 2 37.5 9.6
91 3 35 9.5
Phase I 225 4 39 9.2
2.5 2 4000–4500
continuous 372 5 40.5 9.2
518 6 37.5 10.1
771 7 35.5 10.0
954 8 40.5 10.2
1086 9 50 9.5
1092 10 50.5 9.5
1185 11 46.5 9.4
Plant#1 1316 12 50.5 9.5
1428 13 52 9.5
1548 14 49 9.5
1676 15 50.5 9.3
Phase II
1807 16 (ˆ) 2 52.5 9.4 4000–4500
semi-batch
2004 17 51 9.5
2215 18 49 9.3
2354 19 51.5 9.2
2563 20 50 9.3
2739 21 49.5 9.3
2927 22 49.5 9.3
3081 23 48.5 9.2
Semi-batch * 0 1 (ˆˆ) 6 52 9.4–10.1 500
3 2 48 9.5–10.1
18 3 53 9.4 **
59 4 46 9.2 **
Plant#2 116 5 45 9.2 **
Continuous 2.2 6 500–700
232 6 55 9.5 **
234 7 56 10.6
280 8 58 10.5
HRT: Hydraulic Retention Time, (ˆ) treated volume: 5 m3 , (ˆˆ) treated volume: 13.2 m3 , * preliminary test,
** no dosage of an alkaline reagent.

In order to evaluate the influence of operating parameters on the ammonia removal in plant #2,
a deeper study based on a two-level factorial experiment is developed. The development of the factorial
experimentation was focused on three operating parameters: temperature, digestate flowrate, and air
flowrate. The pH was not modified with an alkaline reagent dosage. In this case, the stabilization of
pH (at 9.2 to 9.3) is due to the equilibrium obtained from CO2 and ammonia removal. This choice
is due to the high concentration of bicarbonate ion in the solution fed to the plants. In fact, the high
concentration of bicarbonate ion (0.32 N) involves that the increase (with NaOH solution) of digestate
pH more than 9.2 is too expensive and the stabilization of pH (without a reagent dosage) to a pH
of 9.2 to 9.3 (from 7.7 to 7.8), due to the CO2 removal obtained from the bicarbonate decomposition,
is favored.
The variation of operating parameters in the factorial experimentation is reported in Table 4.
All tests were carried out in a continuous mode with an HRT (Hydraulic Retention Time) equal to 6 h
for a higher digestate flowrate (2.2 m3 h−1 ) and 9.5 h for a lower flowrate (1.4 m3 h−1 ).

269
Sustainability 2018, 10, 3073

Table 4. Operative conditions of factorial experimentation (plant #2).

Temperature [◦ C] Air Flowrate [Nm3 h−1 ] Digestate Flowrate [m3 h−1 ]

1.4
500
2.2
50
1.4
700
2.2
1.4
500
2.2
60
1.4
700
2.2

With regard to the deepening study based on a two-level factorial experiment, the correlation
between the real removal yields of ammonia (RR ) and the values estimated (RS ) with two linear models
is considered.
The aim of this study is to evaluate the effects of the operating parameters tested (temperature,
digestate flowrate, and air flowrate) on ammoniacal nitrogen removal yields by the use of a simple
linear model in which no constant is present: the hypothesis is RS = RR for RR = 0.
The following linear model was applied below.

RS = a T + b Qa + c Qd (1)

where T is the temperature [◦ C], Qa is the air flowrate [Nm3 h−1 ], Qd is the digestate flowrate [m3 h−1 ],
and a, b, and c are the weights of the operating parameters reported above.
In addition, a more complex linear model is proposed. In this case, the correlation between the
operating parameters at two and three levels is taken into account.

RS = a T + b Qa + c Qd + d T Qa + e T Qd + f Qa Qd + g T Qa Qd (2)

3. Results
The results of the tests carried out on plant #1 and plant #2 are reported in this section. In particular,
the effects of different operative conditions on the ammonia removal yields are shown. Moreover,
the results of a two-level factorial experiment (carried out on plant #2) are reported in order to study
the influence of operating parameters on the ammonia removal in plant #2.

3.1. Plant #1 Results

Figure 3 reports pH and temperature in the stripping reactor and the trend of both ammoniacal
nitrogen input and output concentrations during the working of plant #1 (both in a continuous and a
semi-batch mode). Moreover, in Figure 4, the ammonia removal yields are reported.
As shown in these figures, the removal yields on plant #1 that works in a continuous mode (like a
rear-mixed plug-flow column) varied from 22% to 37%. In these conditions (phase I), the system has a
low efficiency. Low enhancement of ammonia removal yields (mean values from 25% up to 34%) can
be obtained only by increasing the dosages of an alkaline reagent by 2 to 2.5 times (as shown by tests
#6, #7, and #8 in which the pH rises from mean values of 9.4—in tests #1 to #5—up to 10.1).
When plant #1 worked in semi-batch conditions (phase II) and a pH similar to the first period of
phase I (mean value of 9.4) performance increased, the ammonia removal yields raised from 25% (mean
value of the first period of phase I) to 66% (tests #14). Moreover, in these conditions, the operative pH
has been obtained with a lower dosage of an alkaline reagent (less than about 30%) with respect to a
continuous mode (phase I).

270
Sustainability 2018, 10, 3073

Figure 3. Plant #1 results: input and output ammoniacal nitrogen concentrations and pH and
temperature in the stripping reactor.

According to the Henry law on gas/liquid equilibrium of ammonia/water system, in the same
conditions, the ammonia removal yields increase with a rising temperature. As expected, in Figure 4b,
the performance enhancement of the system vs. temperature can be observed. The low value of the
correlation index (R2 ) equal to 0.19 point out that, in addition to the temperature, several operative
parameters (that are controlled such as pH or uncontrolled such as fouling) have an important effect
on the results.
The influence of these parameters is more evident in Figure 4a in which the decrease of ammonia
removal yields seems be due to the temperature increasing.
The results reported in Figure 4 show that an increase in the ammonia removal yields from 25%
to 62% (mean values) can be observed when the temperature increases from the mean values of 38 ◦ C
(Figure 4a) to 50 ◦ C (Figure 4b). These results are consistent with the Henry law and with the work
conditions that changed from a continuous to a semi-batch mode.

Figure 4. Plant #1 results: ammonia removal yields.

271
Sustainability 2018, 10, 3073

3.2. Plant #2 Results

Regarding plant #2, Table 5 shows the trend of the input and output ammoniacal nitrogen
concentrations and the removal yields obtained during continuous and semi-batch (for preliminary
test only) conditions. The operating temperature and pH are also reported.

Table 5. Plant #2 results.

Ammoniacal
Work
Day Test # Temperature [◦ C] pH
Type of Alkaline Concentration [g L−1 ] Removal
Condition Reagent Yield [%]
IN OUT
Semi-batch 0 1 52 9.4–10.1 NaOH 2.75 0.57 79
3 2 48 9.5–10.1 NaOH 2.12 0.81 62
18 3 53 9.4 - 2.18 1.32 39
59 4 46 9.2 - 2.53 1.94 23
Continuous 116 5 45 9.2 - 2.61 1.82 30
232 6 55 9.5 - 2.65 1.61 39
234 7 56 10.6 NaOH 2.71 1.12 59
280 8 58 10.5 NaOH 2.64 0.91 66

In the preliminary test (in the semi-batch mode), the ammonia removal yield is equal to 79%.
The lower ammonia removal yields (from 23% to 39%) are obtained in a continuous mode with
a temperature ranging from 45 to 55 ◦ C and with pH ranging from 9.2 to 9.5 (obtained without an
alkaline reagent dosage). Moreover, the increase of temperature and pH improves the performance.
An ammonia removal yield of 66% was reached when operating at 58 ◦ C and a pH equal to 10.5.
It can be noted that the high bicarbonate concentrations in the digestate fed to the stripping reactor
with the temperature increasing by 45 to 55 ◦ C allow us to work with a pH from 9.2 to 9.5 without the
dosage of a strong alkaline reagent. This behavior is due to the thermal decomposition of bicarbonates
in carbonates with the development of CO2 , which is subsequently removed from the aqueous phase.
When the pH value is 9.3 to 9.5, the concentration of un-dissociated ammonia (also known as free
ammonia nitrogen) is about 40% while the ammonium ion content (NH4 + ) is 60%. The increase of pH
up to the value of 10.5 significantly enhances the performance by raising the free ammonia nitrogen
percentage up to values close to 100%.
Regarding the study based on a two-level factorial experimentation, the results (in terms of real
removal yields of ammonia—RR ) are reported in Table 6.

Table 6. Results of two-level factorial experimentation (plant #2).

Temperature Air Flowrate Digestate Flowrate Real Removal Yields of Ammonia (RR )
[◦ C] [Nm3 h−1 ] [m3 h−1 ] [%]
1.4 32.7
1.4 30.9
500
2.2 25.4
2.2 27.2
50
1.4 42.1
1.4 43.0
700
2.2 45.8
2.2 44.1
1.4 48.9
1.4 48.6
500
2.2 35.3
2.2 37.3
60
1.4 44.8
1.4 44.9
700
2.2 40.7
2.2 38.2

272
Sustainability 2018, 10, 3073

The results of the simple linear model (Equation (1)), obtained by the minimization of the squared
error sum (RR − RS )2 , are the following: a = 0.711, b = 0.0228, and c = −7.88.
Regarding the more complex linear model (Equation (2)), the results are: a = 1.898, b = −0.2387,
c = −8.4630, d = 0.00253, e = −0.6221, f = 0.1297, and g = −0.0012.
In Figure 5, the correlations between RR and RS for both models are reported. Concerning
the linear model described with Equation (1), the slope of the interpolation line is near 0.99.
This result suggests that the operating parameters taken into account play an important role in
process performance (Figure 5a). Despite the fact that the correlation coefficient (R2 ) is not very high
due to the variation of digestate characteristics during the experimentation, the model is able to obtain
a suitable estimation of ammoniacal nitrogen removal yields.

Figure 5. Plant #2 results: correlations between real removal yields (RR ) and the estimated values (RS )
for the models studied.

Regarding the more complex model (Equation (2)), the results obtained (Figure 5b) in terms of a
correlation coefficient are better than the first model. However, the physical meaning of the calculated
weights is very difficult to explain. Therefore, the simple linear model (Equation (1)) is recommended.
The calculated values of weights (a, b, and c) revealed the positive effects of temperature and air
flowrate on the ammonia removal yields while it is observed that the increase of digestate flowrate
(with a reduction of the mean HRT in the stripping reactor) involves a performance reduction.
Since the weights are inversely related to the values of respective operating parameters (T, Qa ,
and Qd ) in order to define the real weight of the variables on the ammoniacal nitrogen removal
yield, which are the coefficients obtained by using the square error sum minimization reported above,
these have been normalized. The coefficients a, b, and c have been multiplied by the 10% of the average
value of the corresponding parameters. The results obtained are: anormalized = 3.91, bnormalized = 1.37,
and cnormalized = −1.42. Therefore, the normalization (to the range 0–100) of the mean values for each
parameter (T = 55 ◦ C, Qa = 600 Nm3 h−1 , Qd = 1.8 m3 h−1 ) was carried out.

4. Discussion
Concerning plant #1, the experimental results show that the main parameters that play an
important role on ammonia removal are work conditions (i.e., semi-batch or continuous mode), pH,
and temperature.

273
Sustainability 2018, 10, 3073

Concerning pH, an increase from 9.4 to 10 involves the enhancement of ammonia removal yields
from 25% to 34%. As confirmed by Guštin and Marinšek-Logar [28], the increase of pH values promote
the ammonia removal but only up to a pH of 10.
The effects of temperature and work conditions are not evaluable individually because the change
from continuous to semi-batch conditions falls with the main increasing of the temperature (from 38 to
50 ◦ C).
The results point out that the work conditions of the plant (i.e., semi-batch or continuous mode)
should be the main parameters that affect the performance of a stripping reactor. We have observed
that, in semi-batch conditions, the ammonia removal yields are higher than 50% with respect to a
continuous mode operation.
The management of plant #1 highlighted the following main issues: high-energy costs and fouling.
The high-energy costs are mainly due to the electrical power required from the radial fan (12 to 14 kW)
and the thermal power (120 kW in winter conditions) for the preheated air supply in the stripping
reactor (4000 to 4500 Nm3 h−1 at 45 ◦ C) by using an air/water exchanger. Furthermore, regarding
the fouling issue, a more efficient digestate pretreatment (with a mesh of 150 μm) with respect to the
conventional solid/liquid separators (screw press or rotary drum) must be applied. Therefore, a better
removal of suspended solids especially with a fibrous matrix can be obtained. The concentration of
suspended solids in the pretreated digestate inlet to stripping column is lower than 1% and the fouling
of packing material is reduced with a significant performance improvement.
Plant #2 worked only in a continuous mode (with the exception of the preliminary test—see
Table 3). The results obtained during the nine months of management (HRT equal to 6 h) with a
temperature variation from 48 to 58 ◦ C (that depends on external weather conditions) showed that the
pH seems to be the main parameter that affects the performance. Therefore, the dosage of NaOH is the
key factor regarding (i) the ammonia removal yields and (ii) the management costs of the plant.
An important result obtained from this work concerns the equilibrium pH, which, as already
pointed out, at a temperature between 45 to 55 ◦ C, autonomously (without the dosage of alkaline
reagent) reaches values from 9.2 to 9.5, i.e., in a suitable range to obtain an efficient ammonia removal
from the aqueous phase. These results are confirmed by previous experimental works [29,30]. However,
this aspect is strictly related to the characteristics of the substrate treated with AD especially to its
alkalinity that depends both on the different feeding substrate and on the anaerobic degradation
process of the same substrate.
In any case, in order to verify this operational feasibility on the digestate treated during this
work, the two-levels of factorial experimentation are based on three parameters (temperature, air
flowrate, and digestate flowrate) was developed. The two-level factorial test has proven that the
temperature is a main parameter when no alkaline reagent is added. In this case, despite the fact that
no statistical analyses have been carried out, the temperature seems to significantly affect the process
performance. In fact, the temperature influences the reaction kinetics and the equilibrium of phase
transfer by an exponential law. However, the other two parameters (air and digestate flowrates) must
be taken into account in order to obtain ammonia removal yields that allow the correct management of
nitrogen content in the digestate. The experiment results suggest the need for a proper management
of available thermal energy with the aim to operate always in optimal conditions with respect to the
process temperature.
The study of plant #2 allows us to confirm the feasibility to work on digestate with high
concentrations of suspended solids without the occurrence of a fouling problem. Moreover, it was
observed that, despite the fact that the high concentration of suspended solids (values higher than
1%) has a negative effect on the rheology, this aspect does not affect the alkaline reagent dosage
to obtain pH values from 10.0 to 10.5. The amount of alkaline reagent significantly influences the
digestate alkalinity.
Concerning economic aspects, the operating cost, in terms of euro per m3 of digestate treated,
related to plant #2 (without the dosage of alkaline reagent) is about one-third of that in plant #1.

274
Sustainability 2018, 10, 3073

The avoided dosage of the alkaline reagent involves a significant cost saving (estimated in 2–3 € per
m3 of digestate). Moreover, regarding the air supply, the electrical power of the rotary lobe compressor
in plant #2 (7–8 kW) is lower than the value required for the radial fan of plant #1 (12–14 kW). Lastly,
regarding plant #1, the semi-batch operative mode seems to be more efficient than the continuous
mode with complete mixing.
Future developments regarding the study of a stripping reactor allowed to treat (with a lower
thermal energy input) livestock manure (or other substrate) with low energy content cannot suitable
for biogas production with anaerobic digestion. In this case, the thermal energy required for the
process could be obtained from the protonation/dissolution reaction of ammonia gas in sulphuric acid.

5. Conclusions
In this work, two different ammonia stripping full-scale plants are studied. The substrate tested is
liquid digestate derived from the anaerobic digestion of livestock manure and corn silage.
Plant #1, based on a packed column, shows low ammonia removal yields (from 22% to 37%) when
it works in a continuous mode. Instead, the semi-batch conditions increase the performance (up to
66%) and reduce the alkaline reagent dosage due to the application of pH significantly lower than the
values maintained in the continuous mode tests (9.2–9.5 with respect to 10–10.2). Despite these results,
the main issues are related to high-energy costs due to the preheated air supply and to the significant
digestate pretreatment required to avoid fouling.
Therefore, plant #2, based on an air bubble reactor without filling material, was studied. The lower
performance (ammonia removal yields from 23% to 39%) were obtained in a continuous mode with
temperatures ranging from 45 to 55 ◦ C and, without an alkaline reagent dosage, pH autonomously
raised from 9.2 to 9.5. When the temperature and pH increase, the performance enhances and reaches
an ammonia removal yield of 66%.
The use of plant #2 allows us to obtain ammonia removal yields up to 50% (with HRT equal to
9.5 h) in a continuous mode. This value is higher than the performance obtained with the use of plant
#1 in a continuous operation. Moreover, the fouling issue is avoided, the air flowrate required is one
order of magnitude lower, and no dosage of NaOH is provided. This aspect is very important because
the digestate with low sodium content can be recovered on agricultural soil avoiding issues concerning
a salinity increase.

Author Contributions: M.B. supervised the experimental activities and data analysis. M.C.C., A.A., and I.B.
performed the results interpretation and the paper drafting.
Funding: This research received no external funding.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Bousek, J.; Scroccaro, D.; Sima, J.; Weissenbacher, N.; Fuchs, W. Influence of the gas composition on the
efficiency of ammonia stripping of biogas digestate. Bioresour. Technol. 2016, 203, 259–266. [CrossRef]
[PubMed]
2. Panepinto, D.; Genon, G.; Brizio, E.; Russolillo, D. Production of green energy from co-digestion: Perspectives
for the Province of Cuneo, energetic balance and environmental sustainability. Clean Technol. Environ. Policy
2013, 15, 1055–1062. [CrossRef]
3. Provenzano, M.R.; Iannuzzi, G.; Fabbri, C.; Senesi, N. Qualitative Characterization and Differentiation of
Digestates from Different Biowastes Using FTIR and Fluorescence Spectroscopies. J. Environ. Prot. 2011,
2, 83–89. [CrossRef]
4. Collivignarelli, M.C.; Bertanza, G.; Abbà, A.; Sordi, M.; Pedrazzani, R. Synergy between Anaerobic
Digestion and a Post-Treatment Based on Thermophilic Aerobic Membrane Reactor (TAMR). Environ. Prog.
Sustain. Energy 2017, 36, 1802–1809. [CrossRef]
5. Möller, K.; Müller, T. Effects of anaerobic digestion on digestate nutrient availability and crop growth:
A review. Eng. Life Sci. 2012, 12, 242–257. [CrossRef]

275
Sustainability 2018, 10, 3073

6. Cornalba, V. Energy Recovery from Biomass: Technical Aspects and Environmental Impact. Ph.D. Thesis,
University of Pavia, Pavia, Italy, 2011.
7. Blumenstein, B.; Siegmeier, T.; Bruckhaus, C.; Anspach, V.; Möller, D. Integrated Bioenergy and Food
Production—A German Survey on Structure and Developments of Anaerobic Digestion in Organic Farming
Systems. Sustainability 2015, 7, 10709–10732. [CrossRef]
8. European Parliament and Council. Council Directive 91/676/EEC of 12 December 1991 Concerning the
Protection of Waters against Pollution Caused by Nitrates from Agricultural Sources. 1991. Available online:
https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A31991L0676 (accessed on 10 July 2018).
9. Italian Parliament. General Criteria and Technical Standards for Regional Regulating Agricultural Use of
Livestock Manure and Wastewater, as Well as for the Production and the Agronomic Use of the Digestate,
Ministerial Decree 25 February 2016. Available online: http://www.gazzettaufficiale.it/eli/id/2016/04/18/
16A02762/sg (accessed on 10 July 2018).
10. Drosg, B.; Fuchs, W.; Al Seadi, T.; Madsen, M.; Linke, B. Nutrient Recovery by Biogas Digestate Processing;
BAXTER, D., Ed.; IEA Bioenergy: Paris, France, 2015; ISBN 978-1-910154-16-8.
11. Gong, H.; Yan, Z.; Liang, K.Q.; Jin, Z.Y.; Wang, K.J. Concentrating process of liquid digestate by disk
tube-reverse osmosis system. Desalination 2013, 326, 30–36. [CrossRef]
12. Jurado, E.; Antonopoulou, G.; Lyberatos, G.; Gavala, H.N.; Skiadas, I.V. Continuous anaerobic digestion
of swine manure: ADM1-based modelling and effect of addition of swine manure fibers pretreated with
aqueous ammonia soaking. Appl. Energy 2016, 172, 190–198. [CrossRef]
13. Mirtsou-Xanthopoulou, C.; Jurado, E.; Skiadas, I.V.; Gavala, H.N. Effect of Aqueous Ammonia Soaking in the
Methane Yield and Composition of Digested Manure Fibers Applying Different Ammonia Concentrations
and Treatment Durations. Energies 2014, 7, 4157–4158. [CrossRef]
14. Yilmazel, Y.D.; Demirer, G.N. Removal and recovery of nutrients as struvite from anaerobic digestion
residues of poultry manure. Environ. Technol. 2011, 32, 783–794. [CrossRef] [PubMed]
15. Uysal, A.; Yilmazel, Y.D.; Demirer, G.N. The determination of fertilizer quality of the formed struvite from
effluent of a sewage sludge anaerobic digester. J. Hazard. Mater. 2010, 181, 248–254. [CrossRef] [PubMed]
16. Provolo, G.; Perazzolo, F.; Mattacchini, G.; Finzi, A.; Naldi, E.; Riva, E. Nitrogen removal from digested
slurries using a simplified ammonia stripping technique. Waste Manag. 2017, 69, 154–161. [CrossRef]
[PubMed]
17. Serna-Maza, A.; Heaven, S.; Banks, C.J. Biogas stripping of ammonia from fresh digestate from a food waste
digester. Bioresour. Technol. 2015, 190, 66–75. [CrossRef] [PubMed]
18. Bonmatì, A.; Campos, E.; Flotats, X. Concentration of pig slurry by evaporation: Anaerobic digestion as the
key process. Water Sci. Technol. 2003, 48, 189–194. [CrossRef] [PubMed]
19. Guercini, S.; Castelli, G.; Rumor, C. Vacuum evaporation treatment of digestate: Full exploitation of
cogeneration heat to process the whole digestate production. Water Sci. Technol. 2014, 70, 479–485. [CrossRef]
[PubMed]
20. Lauterbock, B.; Ortner, M.; Haider, R.; Fuchs, W. Counteracting ammonia inhibition in anaerobic digestion
by removal with a hollow fiber membrane contactor. Water Res. 2012, 46, 4861–4869. [CrossRef] [PubMed]
21. Lauterbock, B.; Moder, K.; Germ, T.; Fuchs, W. Impact of characteristic membrane parameters on the transfer
rate of ammonia in membrane contactor application. Sep. Purif. Technol. 2013, 116, 327–334. [CrossRef]
22. Collivignarelli, M.C.; Abbà, A.; Castagnola, F.; Bertanza, G. Minimization of municipal sewage sludge by
means of a thermophilic membrane bioreactor with intermittent aeration. J. Clean. Prod. 2017, 143, 369–376.
[CrossRef]
23. Collivignarelli, M.C.; Abbà, A.; Bertanza, G.; Setti, M.; Barbieri, G.; Frattarola, A. Integrating novel
(thermophilic aerobic membrane reactor-TAMR) and conventional (conventional activated sludge-CAS)
biological processes for the treatment of high strength aqueous wastes. Bioresour. Technol. 2018, 255, 213–219.
[CrossRef] [PubMed]
24. Zarebska, A.; Romero Nieto, D.; Christensen, K.V.; Søtof Fjerbæk, L.; Norddhal, B. Ammonium Fertilizers
Production from Manure—A Critical Review. Crit. Rev. Environ. Sci. Technol. 2015, 45, 1469–1521. [CrossRef]
25. Limoli, A.; Langone, M.; Andreottola, G. Ammonia removal from raw manure digestate by means of a
turbulent mixing stripping process. J. Environ. Manag. 2016, 176, 1–10. [CrossRef] [PubMed]

276
Sustainability 2018, 10, 3073

26. Piccinini, S.; Moscatelli, G.; Fabbri, C. Nitrogen recovery from digestate with ammonia stripping: Results of 27
tests. In Proceedings of the ManuREsource 2013—Manure Management and Valorization, Bruges, Belgium,
5–7 December 2013; Available online: http://www.crpa.it/media/documents/crpa_www/Convegni/
20131206_manureResource_BELGIO/Piccinini_Ammonia_Stripping.pdf (accessed on 10 July 2018).
27. Fabbri, C.; Piccinini, S. Dairy Cattle and Biogas: Guidelines for the Construction and Management
of Plants. Centro Ricerche Produzioni Animali, S.p.A.: Reggio Emilia, Italy, 2012. (In Italian).
Available online: http://www.crpa.it/media/documents/crpa_www/Pubblicazi/E-book/lineebiogas/
Bovini_da_latte_e_biogas.pdf (accessed on 10 July 2018).
28. Guštin, S.; Marinšek-Logar, R. Effect of pH, temperature and air flow rate on the continuous ammonia
stripping of the anaerobic digestion effluent. Process Saf. Environ. Prot. 2011, 89, 61–66. [CrossRef]
29. Collivignarelli, C.; Baldi, M.; Gorini, R. Ammonia removal from MSW landfill leachate by means of air
stripping. Solid Waste 1992, VI, 1–6. (In Italian)
30. Collivignarelli, C.; Bertanza, G.; Baldi, M.; Avezzù, F. Ammonia stripping from MSW landfill leachate in
bubble reactors: Process modeling and optimization. Waste Manag. Res. 1998, 16, 455–466. [CrossRef]

© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

277
 MDPI
St. Alban-Anlage 66
4052 Basel
Switzerland
Tel. +41 61 683 77 34
Fax +41 61 302 89 18
www.mdpi.com

Sustainability Editorial Office

E-mail: [email protected]
www.mdpi.com/journal/sustainability
MDPI
St. Alban-Anlage 66
4052 Basel
Switzerland
Tel: +41 61 683 77 34
Fax: +41 61 302 89 18
www.mdpi.com ISBN 978-3-03897-553-3