Energies 2011, 4, 804-817; doi:10.

3390/en4050804
OPEN ACCESS

energies
ISSN 1996-1073
www.mdpi.com/journal/energies

Review

Utilization of Natural Farm Resources for Promoting High

Energy Efficiency in Low-Input Organic Farming
Veronica Arthurson * and Lotta Jderlund

Uppsala Biocenter, Department of Microbiology, Swedish University of Agricultural Sciences,

Uppsala, Sweden; E-Mail: [email protected]

* Author to whom correspondence should be addressed; E-Mail: [email protected];

Tel.: +46-18-67-3212; Fax: +46-18-67-3393.

Received: 15 February 2011; in revised form: 10 March 2011 / Accepted: 9 May 2011 /
Published: 12 May 2011

Abstract: Both organic and conventional farming processes require energy input in the
form of diesel fuel for farming equipment, animal feed, and fertilizer compounds. The most
significant difference between the two methods is the use in conventional farming of
mineral fertilizers and pesticides that are minimally employed in organic management. It is
argued that organic farming is more environmentally friendly, given that synthetic
fertilizers mainly used at conventional farms are replaced with animal manure and cover
crops. Nutrient uptake by plants is additionally enhanced by the effective use of rhizobia
and other types of plant growth-promoting bacteria, in combination with arbuscular
mycorrhizal fungi. This article aims to compare the amounts and/or types of energy and
nutrients required for both farming systems and provide feasible suggestions for the
sustainable use of farm resources in combination with good crop yields.

Keywords: energy; nutrient; recycling; organic farming

1. Introduction

Energy is essential for the survival of plants, animals, and microorganisms. Phototrophic plants,
algae and specific bacterial groups can directly collect energy from sunlight to catalyze the conversion
of carbon dioxide into organic molecules. However, animals and other heterotrophs require reduced
carbon compounds for their reproduction and growth, and are hence dependent on phototrophs for
Energies 2011, 4 805

satisfying their energy requirements. Generally, the use of cover crops in farming improves the
capturing of solar energy by plants by 1.8 times [1], in addition to the beneficial nutrient and water
conserving properties [2]. Moreover, leguminous cover crops contribute substantial amounts of
nitrogen to the soil upon tilling [1]. Fossil and solar energy are needed for all types of agricultural
farming, including organic and conventional systems. The major differences in energy requirements
between these farming systems are attributable to the use of mineral fertilizers and pesticides, which
are not allowed on certified organic farms [1].
Agricultural production needs to keep up with the constantly growing human population trend in
order to ensure sufficient food and meet the renewable energy requirements [3]. To date, high crop
yields have been achieved by the inappropriate use of large amounts of chemical fertilizers and
pesticides, previously shown to cause nutrient (e.g., nitrogen (N) and phosphorus (P)) leaching and
runoff [4,5]. Nitrogen levels exceeding 50% of the amounts applied are lost as N2, leached nitrate or
trace gases [4,6], whereas as much as 90% of applied P may precipitate, contributing to P pollution [7,8].
One way to protect the environment through reducing this nutrient leakage from farming systems is by
ensuring the presence of crops in the field when the nutrient is made bioavailable, for example, via
application of cover crops. The negative environmental impact of fertilizers has consistently been ascribed
to the low efficiency of nutrient uptake [9]. One possible way to facilitate environmentally-friendly crop
production with high yield would be via integrated management with no redundant fertilizer
application, instead combining nutrient input with microbes stimulating plant nutrient uptake.
The main aim of this report is to compare conventional and organic farming systems, with emphasis
on the energy required and nutrient sources present in each system. We have additionally evaluated the
potential methods and resources that can be applied and developed further to obtain an optimal
sustainable farming system with high energy efficiency.

2. Concepts in Organic Farming

Recent years have seen a steady growth in the organic farming sector in Europe, with a 21%
increase in the organic farming area in the European Union between 2005 and 2008 [10]. Both farmers
and consumers are concerned with the development of sustainable agriculture, improved animal
welfare and healthiness of consumed food. Moreover, there has been increasing interest in locally
produced food from an environmental perspective [11]. Organic farming is a holistic approach to
agriculture, which takes into account environmental protection, animal welfare and consumer
confidence, meaning that consumers should be able to trust organic products as healthy and fair.
Societal and economical developments are important aspects of organic agriculture. The basic idea of
organic farming is that each farm should be self-supporting, recycling its energy and the nutrients
produced (Figure 1), thus providing an effective and environmentally friendly form of agriculture.
Four principles have been formulated by the International Federation of Organic Agriculture
Movements (IFOAM), termed the principles of health, ecology, fairness and care [12]. The first
principle, dealing with health, may be summarized as a wish to maintain the function and wellbeing of
all ecosystems and organisms living therein. The principle of ecology states that all production should
be based on ecological processes and recycling, and carried out in balance with natural ecosystems in a
way that protects and benefits land, water, air and biodiversity. Fairness and care should be a part of
Energies 2011, 4 806

the process with respect to all parties involved in the production steps, thus ensuring an environment
that can sustain our successors.

Figure 1. Energy and nutrient re-cycling in organic farming. Animal feed and bedding
material are needed in order to keep animals. The farmyard manure can then be stored,
preferably composted to reduce the number of pathogenic bacteria, or used for biogas
production. Nutrient analysis is an important step if the manure is to be used as a fertilizer.
Other types of fertilizers that can be used are cover crops and green manure. If the farm
does not keep animals, or cannot produce enough manure, off-farm manure is sometimes
bought from near-by farms. The application technique as well as the timing and rate of
application, are very important steps to consider to minimize nutrient leaching. Fuels used
for the farming equipment is often of fossil origin, but could in the future consist of biogas,
in order to minimize farm dependence on fossil fuels. Plant growth promoting bacteria and
arbuscular mycorrhizal fungi can be used in crop production to enhance plant nutrient
uptake and to minimize nutrient leaching. The crops produced may then be stored and sold
to consumers or used as feed for the farmyard animals, thus closing the farm energy cycle.

A major proportion of the energy required for both organic and conventional farming systems is
fossil-based (Table 1). This energy is required for machinery fuel as well as indirectly for production
of fertilizer, pesticides and farming equipment [13]. A way of minimizing the use of fossil fuels in
the future would be on-farm biogas production [14], although this is not economically viable at
Energies 2011, 4 807

present [15]. One theory is to produce rapeseed and grass-clover crops in order to maintain soil fertility
and generate biomass for energy production in nearby biogas plants [16].

Table 1. Energy input (total energy costs), reported as GJ ha1 year1, required for different
crop species and farming systems (e.g., organic, integrated and conventional farming,
respectively).
Organic Integrated Conventional Reference
Sugar beet - 26.3 33.8 [17]
Durum wheat - 16.9 27.1 [17]
Sorghum - 16.0 22.9 [17]
Sunflower - 14.8 23.0 [17]
Barley 9.0 - 13.8 [18]
Grain crops 4.8 5.2 7.1 [19]
Spring barley 12.6 - 16.6 [20]
Pea 7.4 - 10.4 [20]
Winter wheat 9.2 - 20.3 [20]
Various crops 8.1 12.4 - [21]
Wheat-potato-clover 13.3 - 24.1 [22]
Raisin 22.2 - 28.9 [23]
Soybean 7.7 13.6 - [24]
Maize 25.9 46.9 - [24]
wheat 11.4 28.0 - [24]
Soybean 9.6 - 8.8 [1]
Grain crops 24.2 - 68.4 [25]

The self-supporting theory that every farm should be a closed system with regard to energy and
nutrients [26] and the concept of avoiding mineral fertilizers have been subjected to considerable
criticism. Kirchmann et al. [26] argue that organic farms are dependent on nutrient and energy input
from conventional farms, for example, in terms of acquiring straw or animal feed, thus relying on
mineral fertilizers as a secondary step. The authors have found no scientific evidence that increased
microbial activity in organically managed soil can compensate for the loss of easily bioavailable
nutrients supplied by mineral fertilizers [26].
However, soil in organic systems generally contains higher organic matter than that in conventional
systems. For example, conventionally managed soil consists of 34% organic matter whereas the
corresponding value for organically managed soil is 5.25.5% [1,2]. Pimentel and co-workers [27]
emphasized that the higher organic matter content in organically managed soil is directly related to its
energy efficiency, as organic matter increases water infiltration leading to reduced soil erosion,
improves soil food webs, and contributes to nitrogen cycling from within the soil [27]. Moreover,
Pimentel et al. [1] compared corn and soybean crops produced in conventional and organic farms. The
conventional farms used mineral fertilizers and pesticides according to U.S. standard dose
recommendations, whereas the organic farms received no additives. The authors reported that
organically produced corn and soybean consumed 30% less fossil energy on average, in combination
with higher degrees of water conservation in the soil, better maintenance of soil quality and
conservation of more biological resources, compared to conventional farming [1].
Energies 2011, 4 808

For effective crop and vegetable production, there is a constant need for nutrient and energy input
into the soil. Mineral fertilizers have negative effects on biogeochemical cycles and enhance leakage of
nutrients, mostly N and P [28]. It is suggested that the natural fertility and health of soil can be restored
without the need for synthetic chemicals by using fertilizers produced on the farm, such as stable
manure, green manure or composted organic material [4]. These organic fertilizers are possibly partly
converted by the soil bacterial and fungal communities to more bioavailable compounds that can be
taken up by plants [29,30]. Crop yield in organic farming may be only 20% lower than that in
conventional farming, with a 3451% decrease in nutrient input (N, P, potassium (K)) over a 21-year
period [22]. Moreover, organically and conventionally produced corn, soybean and wheat have shown
no significant differences in yield after a 4-year transition period to organic farming [1]. Certain
microbial inoculants consisting of arbuscular mycorrhizal fungi (AMF), plant growth-promoting
rhizobacteria (PGPR) and nitrogen-fixing bacteria enhance nutrient uptake among plants [30]. Nutrient
balance in organic farms is around zero (N, P, K), with a negative balance for P and K, and review of
energy consumption shows that organic farms consume less energy than conventional farms [31],
along with higher energy efficiency of annual and permanent crop production (Table 2).

Table 2. Energy efficiency values, calculated as the ratio between the crop production
energy output and the energy input, for different species in various cropping systems
(e.g., OF, organic farming; IF, integrated farming; CF, conventional farming).
Energy Energy Energy
Duration
Crop Country Efficiency, Efficiency, Efficiency, Reference
(years)
OF IF CF
Apricot Turkey 3 2.2 - 1.5 [23]
Sugar beet Italy 12 - 2.9 2.6 [17]
Durum wheat I Italy 12 - 7.5 5.1 [17]
Durum wheat II Italy 12 - 6.9 4.7 [17]
Sorghum Italy 12 - 14.1 10.1 [17]
Sun flower Italy 12 - 17.6 11.4 [17]
Winter rye Germany 5 34.8 23.7 20.9 [21]
Winter rye Germany 5 44.1 22.7 - [21]
Corn US 22 7.7 - 5.1 [1]
Soybean US 22 3.8 - 4.6 [1]
Spring barley Slovakia 11 10.9 - 10.0 [20]
Pea Slovakia 11 12.8 - 9.4 [20]
Winter wheat Slovakia 11 16.4 - 8.2 [20]
Rice Philippines >3 12.7 7.0 4.7 [32]
Grain crops US 17 11 13 10 [19]

3. Microorganisms Stimulating Plant Nutrient Uptake

An interesting alternative is to use mixed microbial inoculants consisting of arbuscular mycorrhizal

fungi (AMF) and plant growth-promoting rhizobacteria (PGPR) [3] to improve crop productivity. Both
AMF and PGPR contribute to enhanced nutrient uptake by plants [33], and the combined effects may
be more pronounced. For example, PGPR may support AM symbiosis by increasing the amount of
Energies 2011, 4 809

bioavailable phosphate. In soil with low P availability, free-living phosphate-solubilizing bacteria

release phosphate ions from sparingly soluble inorganic and organic P compounds [34], contributing to
the soil phosphate pool available for extraradical AM fungal hyphae to forward to the roots [35].
Linderman showed a strong stimulatory effect of PGPR on AM fungal growth [36], whereas Azcn
reported induction of growth of mycelia from Glomus mosseae spores by an identified PGPR [37].
Co-inoculation of selected PGPR and AMF may thus be applied to optimize the formation and
function of AM symbiosis. Despite considerable research focus on the interactions between specific
strains of PGPR and AMF in plant growth promotion, the mechanisms underlying these associations
are not well understood at present. It is suggested that AMF acts as a vehicle for the bacteria [3840],
facilitating transferral between the roots. Further insight into the mechanisms of AMF-PGPR
interactions should facilitate the development of optimized mixed inocula that can be used efficiently
as tools for increasing crop yield.
N2-fixing bacteria improve the bioavailability of N to plants that may be further enhanced when
plants are also colonized by AMF [41]. In terms of N2-fixing rhizobia, mycorrhizal and root nodule
symbioses are typically synergistic, both with regard to infection rate and impact on mineral nutrition
and growth of plants. One possible explanation for the increased N2 fixation in plants colonized by
AMF is that when both N and P are limiting, AMF improves P uptake by the plant, leading to more
available energy for N fixation by the rhizobia [42,43]. Moreover, recent studies have shown that
specific AMF can use decomposing organic N sources for their own nutritional demands and growth,
thus acting as potential N competitors of associative plants [44].
Considering the importance of host plant P status on AM symbiosis, P fertilizers may have a strong
effect on the association between plants and AMF [29]. In intensive conventional farming systems,
application of P fertilizer may lead to surplus of P that largely exceeds crop need, resulting in
accumulation of total and bioavailable P in the soil [4548]. This may lead to less reliance of plants on
AM symbiosis, and consequently, lower colonization levels and propagule sizes [29]. Severe effects of
N-based mineral fertilizer on AM colonization have additionally been reported [4952], inconsistent
with other findings [53,54]. However, organic nutrient sources, such as those applied in organic
farming, are reported to stimulate AMF [49,5562], further emphasizing the importance of maintaining
a healthy soil microbial community. The issue of whether specific indigenous microorganisms should
be selectively stimulated in soil or selected microbial strains added in the form of mixed inocula to
large-scale crop fields remains to be established.

4. Animal WasteA Farm Resource

Prior to the technological advances during World War II, most farmers used an organic way of
producing their crops. However, the new possibilities to use large-scale irrigation, inorganic fertilizers
and chemical pesticides resulted in a growing interest in chemical rather than organic farming. This
kind of intensive agriculture has certainly increased crop yields but meanwhile implied significant
environmental problems [22,63]. Moreover, mineral fertilizers and chemical pesticides tend to be more
energy-consuming than organic products (Table 1). Consequently, increasing numbers of farmers are
once again becoming conscious that animal waste produced on the farm can be of significant value. It
is widespread practice for organic crop and animal farmers to cooperate, providing each other with
Energies 2011, 4 810

straw, animal feed and manure to increase crop yield. Farmyard manure application, one of the most
common strategies used by organic farmers to increase and maintain soil fertility [64], mainly acts as
an important soil nitrogen source, and significantly contributes to nitrate and phosphorus leaching if
not applied appropriately [65]. Since manure contains lower amounts of easily available nutrients than
mineral fertilizers and differs between distinct animal types, farms and years, it is more difficult to
calculate the appropriate application amounts and rates [65]. In order to minimize risks with nutrient
leaching and to maximize plant uptake it is important to evaluate the rate and timing of manure land
application. Which method to use and when to apply the manure depend on several factors, including
cropping and managment systems, climate, type of animal waste and equipments used. In cropping
systems it is important to apply the manure when the nutrients can be optimally used by the crops,
which is often immediately before planting or sowing [65]. Leaching of nutrients is also depending on
the time interval between fertilizer application and the first rainfall. Smith et al. [66] found that one
week was sufficient for minimizing risk of leaching when swine and poultry manure was applied to
soil. Different application techniques can affect the nutrient efficiency, such as different injection
methods which minimize emission of ammonia [67].
A long-term field trial in Switzerland showed that after 21 years, the soil was positively affected by
manure amendment, with increased biomass and microbial activities in organic systems, supporting the
theory of increased nutrient turnover rates in organic farming [64]. However, while animal manure
may be a suitable fertilizer, it is extremely important that care is taken to avoid soil and plant
contamination with human pathogenic bacteria often present in untreated manure [68]. Adequate
composting techniques for animal manure present an effective way of reducing high levels of human
pathogenic bacteria [69]. One should also consider that specific bacterial strains, for example, E. coli
O157:H7, remain longer in manure than in live animals, and thus, insufficiently treated manure is a
potential source of reinfection of livestock with pathogens [70]. Consequently, proper composting
procedures should be carefully optimized according to both duration and internal conditions within the
pile. Manure is an important source of organic matter and nutrients, especially in organic farming
where mineral fertilizers are not allowed. The risk for human pathogenic bacterial contamination of
plants is highest where the produce is likely to be eaten raw (such as in the case of salads, fruit,
spinach, and various vegetables) [71], but should also be taken into consideration for other types of
crops where the risks are less well investigated. Previously, we examined the ability of Salmonella and
Campylobacter strains to persist in manure and soil and disseminate to spinach plants. In many cases,
the pathogens spread from manure to roots, and the pathogenic bacterial content in soil and on spinach
leaves remained relatively constant during the entire evaluation period of 21 days [72,73]. On the other
hand, other studies have shown a progressive decline of pathogenic bacteria, including Escherichia coli
populations, in soil and manure [74]. Semenov et al. [75] demonstrated that the temperature conditions
affect the survival of E. coli O157:H7 in manure, with lower survival under fluctuating than constant
temperatures. In leafy vegetable crops, such as spinach and lettuce, the edible parts come in direct
contact with the soil, thus presenting a significant risk for potential contamination. For example,
organically produced lettuce was previously associated with two outbreaks of Escherichia coli
O157:H7, probably contaminated through cow manure [76]. Organically managed soil is traditionally
associated with higher biodiversity, compared to conventionally managed soil, and ecosystems with
more diverse microbial communities are more resistant to perturbations [77]. This means that organic
Energies 2011, 4 811

crops are less susceptible to infection by human pathogenic bacteria introduced in the manure,
compared to conventional agricultural systems [78,79] to which chemical pesticides and mineral
fertilizers have been added. Moreover, natural soil processes, including symbiotic relationships, local
decomposition processes and nitrogen fixation can be disturbed by also other types of invasive
microorganisms, potentially posing a threat against the stability of the ecosystem [80].

5. Green Manure and Cover CropsRecycling of Plant Material

Cover crops are plants grown in high numbers to protect the soil, thereby minimizing leaching of
nutrients. Legumes employed as cover crops can be used to fix nitrogen together with rhizobium
bacteria, increasing the available soil N for adjacent plants [81]. Cover crops tilled into the soil
function as green manure, and additionally minimize soil erosion and retention of soil moisture,
leaving less space for weeds if maintained all season and improving soil structure [82]. The use of
cover crops have been shown to increase the amount of soil organic C in rye and vetch/rye systems [83]
and affect the nitrogen content and yield of maize [84]. However these effects can vary depending on
the choice of cover crop [85]. For example, beneficial effects on soil organic matter content, a higher
microbial respiration and microbial biomass were detected in a vineyard experiment in California [86].
One limitation of cover crops is the need for increased irrigation, which is a particular problem in dry
areas [82]. The effects of green manure on nitrogen accumulation are usually highest on loamy soils
due to their fertile, moist and nutrient-rich nature [87]. An Irish study has shown that upon growth of a
combination of mustard cover crop with spring barley, the soil solution concentration of NO3 was
between 38 and 70% lower than that without cover crop. Moreover, the total N content lost over winter
was between 18 and 83% lower in the presence of cover crops [88]. Tonitto et al. [89] performed a
metastudy comprising several studies that compared conventional N fertilization with cover crops in
terms of crop yield, nitrate leaching and soil nitrate. When legume cover crops were used (with no
mineral N added), yields were around 10% lower, compared to that in conventional systems with
mineral N fertilization, but with 40% reduction in nitrate leaching on average. Non-legume cover crops
with mineral N amendment showed no decrease in crop yield and 70% reduction in nitrate leaching.
These findings suggest that diversified crop rotation using cover crops can be used to reduce
N-leaching while maintaining acceptable crop yields [89]. However, the results may depend on several
factors, such as type of irrigation [90], climate and soil [87]. In view of these complex interactions, it is
important to investigate each situation and determine the most suitable combination for each climate,
crop and cover plant.

6. Conclusions and Proposals

The main difference in energy and nutrient requirements between organic and conventional farming
is the use of chemical fertilizers and pesticides in the latter system. Organic crop yields are often but
not always smaller than conventional yields, and may be optimized using accurate fertilization regimes
adjusted for each specific site, crop and type of fertilizer. The timing and rate of manure application is
crucial to avoid unnecessary nutrient leaching and use of beneficial microorganisms to enhance plant
nutrient uptake is another way of minimizing environmental damage by nutrient leaching and run-off
loss. Cover crops are also employed to decrease leaching of nutrients and function as green manure if
Energies 2011, 4 812

tilled into the soil, but an effective cover crop must be evaluated in advance together with the
economic crop on the farm site. Recycling of on-farm manure is an effective way of utilizing energy
and nutrients that would otherwise be wasted, but must be performed with care, since pathogenic
bacteria could disseminate into the environment or crops if not handled properly. An efficient way of
reducing the amount of pathogenic bacteria is to compost manure. In the future, energy-efficient
agriculture may be achieved by integrating the organic and conventional farming forms. On-farm
biogas plants are available to further decrease farm dependence on fossil fuels, even if this requires
considerable funding and technical skills. Combination of small amounts of mineral fertilizer, where
necessary, with the use of beneficial microorganisms to increase nutrient uptake could aid in
optimizing crop yield without significant consumption of the available environmental resources.

References

1. Pimentel, D.; Hepperly, P.; Hanson, J.; Seidel, R.; Douds, D. Environmental, energetic, and
economic comparisons of organic and conventional farming systems. Bioscience 2005, 55,
573582.
2. Troeh, F.R.; Hobbs, J.A.; Donahue, R.L. Soil and Water Conservation; Prentice Hall: Upper
Saddle, NJ, USA, 1999.
3. Berg, G. Plant-microbe interactions promoting plant growth and health: perspectives for
controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 2009, 84, 1118.
4. Tilman, D. The greening of the green revolution. Nature 1998, 396, 211212.
5. Gyaneshwar, P.; Kumar, G.N.; Parekh, L.J.; Poole, P.S. Role of soil microorganisms in improving
P nutrition of plants. Plant Soil 2002, 245, 8393.
6. Vitousek, P.M.; Aber, J.D.; Howarth, R.W.; Likens, G.E.; Matson, P.A.; Schindler, D.W.;
Schlesinger, W.H.; Tilman, D.G. Human alteration of the global nitrogen cycle: Sources and
consequences. Ecol. Appl. 1997, 7, 737750.
7. Rodriguez, H.; Fraga, R. Phosphate solubilizing bacteria and their role in plant growth promotion.
Biotechnol. Adv. 1999, 17, 319339.
8. Sharpley, A.N.; Weld, J.L.; Beegle, D.B.; Kleinman, P.J.A.; Gburek, W.J.; Moore, P.A., Jr.;
Mullins, G. Development of phosphorus indices for nutrient management planning strategies in
the United States. J. Soil Water Conserv. 2003, 58, 137152.
9. Barlog, P.; Grzebisz, W. Effect of timing and nitrogen fertilizer application on winter oilseed rape
(Brassica napus L.). II. Nitrogen uptake dynamics and fertilizer efficiency. J. Agron. Crop Sci.
2004, 190, 314323.
10. Eurostat Press Office. Organic Area up by 21% in the EU between 2005 and 2008. Available
online: http://epp.eurostat.ec.europa.eu/cache/ITY_PUBLIC/5-01032010-BP/EN/5-01032010-BP-
EN.PDF (accessed on 18 December 2010).
11. Arthurson, V. Closing the global energy and nutrient cycles through application of biogas residue
to agricultural landPotential benefits and drawback. Energies 2009, 2, 226242.
12. Luttikholt, L.W.M. Principles of organic agriculture as formulated by the international federation
of organic agriculture movements. NJASWagen. J. Life Sci. 2007, 54, 347360.
Energies 2011, 4 813

13. Woods, J.; Williams, A.; Hughes, J.K.; Black, M.; Murphy, R. Energy and the food system. Phil.
Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 29913006.
14. Oleskowicz-Popiel, P. Biogas and bioethanol in organic farming. Ph.D. Thesis, Information
Service Department, Technical University of Denmark, Lyngby, Denmark, 2010.
15. Fredriksson, H.; Baky, A.; Bernesson, S.; Nordberg, .; Norn, O.; Hansson, P.A. Use of on-farm
produced biofuels on organic farmsEvaluation of energy balances and environmental loads for
three possible fuels. Agric. Syst. 2006, 89, 184203.
16. Halberg, N.; Dalgaard, R.; Olesen, J.E.; Dalgaard, T. Energy self-reliance, net-energy production
and GHG emissions in Danish organic cash crop farms. Renew. Agric. Food Syst. 2008, 23, 3037.
17. Nassi O Di Nasso, N.; Bosco, S.; Di Bene, C.; Coli, A.; Mazzoncini, M.; Bonari, E. Energy
efficiency in long-term Mediterranean cropping systems with different management intensities.
Energy 2011, 36, 19241930.
18. Jrgensen, U.; Dalgaard, T.; Kristensen, E.S. Biomass energy in organic farmingthe potential
role of short rotation coppice. Biomass Bioenerg. 2005, 28, 237248.
19. Gelfand, I.; Snapp, S.S.; Robertson, G.P. Energy efficiency of conventional, organic, and
alternative cropping systems for food and fuel at a site in the U.S. Midwest. Environ. Sci.
Technol. 2010, 44, 40064011.
20. Klimekov, M.; Lehock, Z. Comparison of organic and conventional farming system
in term of energy efficiency. 2007. Available online: http://orgprints.org/view/projects/
wissenschaftstagung-2007.html (accessed on 9 March 2011).
21. Deike, S.; Pallut, B.; Christen, O. Investigations on the energy efficiency of organic and
integrated farming with specific emphasis on pesticide use intensity. Eur. J. Agron. 2008, 28,
461470.
22. Mder, P.; Fliessbach, A.; Dubois, D.; Gunst, L.; Fried, P.; Niggli, U. Soil fertility and
biodiversity in organic farming. Science 2002, 296, 16941697.
23. Gndogmus, E.; Bayramoglu, Z. Energy input use on organic farming: A comparative analysis on
organic versus conventional farms in Turkey. J. Agron. 2006, 5, 1622.
24. Sartori, L.; Basso, B.; Bertocco, M.; Oliviero, G. Energy use and economic evaluation of a three
year crop rotation for conservation and organic farming in NE Italy. Biosyst. Eng. 2005, 91,
245256.
25. Hoeppner, J.W.; Entz, M.H.; McConkey, B.G.; Zentner, R.P.; Nagy, C.N. Energy use and
efficiency in two Canadian organic and conventional crop production systems. Renew. Agric.
Food Syst. 2005, 21, 6067.
26. Kirchmann, H.; Ktterer, T.; Bergstrm, L. Nutrient Supply in Organic AgriculturePlant
Availability, Sources and Recycling. In Organic Crop ProductionAmbitions and Limitations;
Kirchmann, H., Bergstrm, L., Eds.; Springer: Dordrecht, The Netherlands, 2008; pp. 89116.
27. Pimentel, D. Impacts of Organic Farming on the Efficiency of Energy Use in Agriculture. An
Organic Center State of Science Review; The Organic Center: Boulder, CO, USA, 2006.
28. Oenema, O. Governmental policies and measures regulating nitrogen and phosphorus from animal
manure in European agriculture. J. Anim. Sci. 2004, 82, 196206.
29. Gosling, P.; Hodge, A.; Goodlass, G.; Bending, G.D. Arbuscular mycorrhizal fungi and organic
farming. Agric. Ecosyst. Environ. 2006, 113, 1735.
Energies 2011, 4 814

30. Adesemoye, A.O.; Kloepper, J.W. Plant-microbes interactions in enhanced fertilizer-use

efficiency. Appl. Microbiol. Biotechnol. 2009, 85, 112.
31. Stolze, M.; Piorr, A.; Hring, A.; Dabbert, S. The Environmental Impacts of Organic Farming in
Europe. In Organic Farming in Europe: Economics and Policy; Dabbert, S., Lampkin, N.,
Michelsen, J., Nieberg, H., Zanoli, R., Hring, A., Eds.; University of Hohemheim: Stuttgart,
Germany, 2000; Volume 6.
32. Mendoza, T.C. Comparative productivity, profitability and energy use in organic, LEISA and
conventional rice production in the Philippines. Livest. Res. Rural Dev. 2002, 14. Available
online: http://www.lrrd.org/lrrd14/6/mend146.htm (accessed on 9 March 2011).
33. Artursson, V.; Finlay, R.D.; Jansson, J.K. Interactions between arbuscular mycorrhizal fungi and
bacteria and their potential for stimulating plant growth. Environ. Microbiol. 2006, 8, 110.
34. Kucey, R.M.N.; Janzen, H.H.; Leggett, M.E. Microbiologically Mediated Increases in
Plant-Available Phosphorus. In Advances in Agronomy; Brady, N.C., Ed.; Academic Press: New
York, NY, USA, 1989; pp. 199228.
35. Smith, S.E.; Read, D.J. Mycorrhizal Symbiosis; Academic Press: San Diego, CA, USA, 1997.
36. Lindermann, R.G. Mycorrhizal interactions with the rhizosphere microflora: The mycorrhizosphere
effect. Phytopathology 1988, 78, 366371.
37. Azcn, R. Germination and hyphal growth of Glomus mosseae in vitro: Effects of rhizosphere
bacteria and cell-free culture media. Soil Biol. Biochem. 1987, 19, 417419.
38. Kim, K.Y.; Jordan, D.; McDonald, G.A. Effect of phosphate-solubilising bacteria and
vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol. Fertil. Soils
1998, 26, 7987.
39. Bianciotto, V.; Bonfante, P. Arbuscular mycorrhizal fungi: A specialized niche for rhizospheric
and endocellular bacteria. Anton. Leeuwenhoek 2002, 81, 365371.
40. Morrissey, J.P.; Dow, M.; Mark, G.L.; OGara, F. Are microbes at the root of a solution to world
food production? Rational exploitation of interactions between microbes and plants can help to
transfrom agriculture. EMBO Rep. 2004, 5, 922926.
41. Barea, J.M.; Azcn, R.; Azcn-Aguilar, C. Mycorrhizosphere interactions to improve plant fitness
and soil quality. Anton. Leeuwenhoek 2002, 81, 343351.
42. Fitter, A.H.; Garbaye, J. Interactions between mycorrhizal fungi and other soil organisms. Plant
Soil 1994, 159, 123132.
43. Kucey, R.M.N.; Paul, E.A. Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and
nodulated faba beans (Vicia faba L.). Soil Biol. Biochem. 1982, 14, 407412.
44. Hodge, A.; Fitter, A.H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from
organic material has implications for N cycling. Proc. Nat. Acad. Sci. USA 2010, 107, 1375413759.
45. Boehm, M.M.; Anderson, D.W. A landscape-scale study of soil quality in three prairie farming
systems. Soil Sci. Soc. Am. J. 1997, 61, 11471159.
46. Withers, P.J.A.; Edwards, A.C.; Foy, R.H. Phosphorus cycling in UK agriculture and implications
for phosphorus loss from soil. Soil Use Manag. 2001, 17, 139149.
47. DeClerck, F.; Singer, M.J.; Lindert, P. A 60-year history of California soil quality using paired
samples. Geoderma 2003, 114, 215230.
Energies 2011, 4 815

48. Kogelmann, W.J.; Lin, H.S.; Bryant, R.B.; Beegle, D.B.; Wolf, A.M.; Petersen, G.W. A statewide
assessment of the impacts of phosphorus-index implementation in Pennsylvania. J. Soil Water
Conser. 2004, 59, 918.
49. Miller, R.L.; Jackson, L.E. Survey of vesicular-arbuscular mycorrhizae in lettuce production in
relation to management and soil factors. J. Agric. Sci. 1998, 130, 173182.
50. Liu, A.; Hamel, C.; Hamilton, R.I.; Ma, B.L.; Smith, D.L. Acquisition of Cu, Zn, Mn and Fe by
mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels.
Mycorrhiza 2000, 9, 331336.
51. Burrows, R.L.; Pfleger, F.L. Arbuscular mycorrhizal fungi respond to increasing plant diversity.
Can. J. Bot. 2002, 80, 120130.
52. Treseder, K.K.; Allen, M.F. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal
fungi, a model and field test. New Phytol. 2002, 155, 507515.
53. Ryan, M.H.; Ash, J. Effects of phosphorus and nitrogen on growth of pasture plants and VAM
fungi in SE Australian soils with contrasting fertiliser histories (conventional and biodynamic).
Agric. Ecosyst. Environ. 1999, 73, 5162.
54. Jumpponen, A.; Trowbridge, J.; Mandyam, K.; Johnson, L. Nitrogen enrichment causes minimal
changes in arbuscular mycorrhizal colonisation but shifts community compositionevidence
from rDNA data. Biol. Fertil. Soils 2005, 41, 217224.
55. Harinikumar, K.M.; Bagyaraj, D.J. Effect of cropping sequence, fertilizers and farmyard manure
on vesicular arbuscular mycorrhizal fungi in different crops over three consecutive seasons. Biol.
Fertil. Soils 1989, 7, 173175.
56. Ryan, M.H.; Chilvers, G.A.; Dumaresq, D.C. Colonisation of wheat by VA-mycorrhizal fungi
was found to be higher on a farm managed in an organic manner than on a conventional
neighbour. Plant Soil 1994, 160, 3340.
57. Baby, U.I.; Manibhushanrao, K. Influence of organic amendments on arbuscular mycorrhizal
fungi in relation to rice sheath blight disease. Mycorrhiza 1996, 6, 201206.
58. Dann, P.R.; Derrick, J.W.; Dumaresq, D.C.; Ryan, M.H. The response of organic and
conventionally grown wheat to superphosphate and reactive phosphate rock. Aust. J. Exp. Agric.
1996, 36, 7178.
59. Douds, D.D.; Galvez, L.; Franke-Snyder, M.; Reider, C.; Drinkwater, L.E. Effect of compost
addition and crop rotation point upon VAM fungi. Agric. Ecosyst. Environ. 1997, 65, 257266.
60. Kabir, Z.; OHalloran, I.P.; Fyles, J.W.; Hamel, C. Dynamics of the mycorrhizal symbiosis of
corn (Zea mays L.), effects of host physiology, tillage practice and fertilization on spatial
distribution of extra-radical mycorrhizal hyphae in the field. Agric. Ecosyst. Environ. 1998, 68,
151163.
61. Joner, E.J. The effect of long-term fertilization with organic or inorganic fertilizers on
mycorrhiza-mediated phosphorus uptake in subterranean clover. Biol. Fertil. Soils 2000, 32,
435440.
62. Alloush, G.A.; Clark, R.B. Maize response to phosphate rock and arbuscular mycorrhizal fungi in
acidic soil. Commun. Soil Sci. Plant Anal. 2001, 32, 231254.
Energies 2011, 4 816

63. Pimentel, D.; Harvey, D.; Resosudarmo, P.; Sinclair, K.; Kurz, D.; McNair, M.; Crist, S.;
Shpritz, L.; Fitton, L.; Saffouri, R.; Blair, R. Environmental and economic costs of soil erosion
and conservation benefits. Science 1995, 267, 11171123
64. Fliebach, A.; Oberholzer, H.R.; Gunst, L.; Mder, P. Soil organic matter and biological soil
quality indicators after 21 years of organic and conventional farming. Agric. Ecosyst. Environ.
2007, 118, 273284.
65. Risse, L.M.; Cabrera, M.L.; Franzluebbers, A.J.; Gaskin, J.W.; Gilley, J.E.; Killorn, R.;
Radcliffe, D.E.; Tollner, W.E.; Zhang, H. Land Application of Manure for Beneficial Reuse. In
Animal Agriculture and the Environment: National Center for Manure and Animal Waste
Management White Papers; Rice, J.M., Caldwell, D.F., Humenik, F.J., Eds.; ASABE: St Joseph,
MI, USA, 2006; pp. 283316.
66. Smith, D.R.; Owens, P.R.; Leytem, A.B.; Warnemuende, E.A. Nutrient losses from manure and
fertilizer applications as impacted by time to first runoff event. Environ. Pollut. 2007, 147, 131137.
67. Nyord, T.; Sgaard, H.T.; Hansen, M.N.; Jensen, L.S. Injection methods to reduce ammonia
emission from volatile liquid fertilisers applied to growing crops. Biosyst. Eng. 2008, 100, 235244.
68. Guan, T.Y.; Holley, R.A. Pathogen survival in swine manure environments and transmission of
human enteric illnessA review. J. Environ. Qual. 2003, 32, 383392.
69. Nicholson, F.A.; Groves, S.J.; Chambers, B.J. Pathogen survival during livestock manure storage
and following land application. Bioresour. Technol. 2005, 96, 135143.
70. Kudva, I.T.; Blanch, K.; Hovde, C.J. Analysis of Escherichia coli O157:H7 survival in ovine or
bovine manure and manure slurry. Appl. Environ. Microbiol. 1998, 64, 31663174.
71. Semenov, A.V. Ecology and modelling of Escherichia coli O157:H7 and Salmonella enterica
serovar typhimurium in cattle manure and soil. Ph.D. Thesis, Wageningen University,
Wageningen, The Netherlands, 2008.
72. Jderlund, L.; Sessitsch, A.; Arthurson, V. Persistence of two Camylobacter jejuni strains in soil
and on spinach plants. Appl. Environ. Soil Sci. 2011, in press.
73. Arthurson, V.; Sessitsch, A.; Jderlund, L. Persistence and spread of Salmonella enterica serovar
Weltevreden in soil and on spinach plants. FEMS Microb. Lett. 2011, 314, 6774.
74. van Elsas, J.D.; Semenov, A.V.; Costa, R.; Trevors, J.T. Survival of Escherichia coli in the
environment: fundamental and public health aspects. ISME J. 2011, 5, 173183.
75. Semenov, A.V.; van Bruggen, A.H.C.; van Overbeek, L.; Termorshuizen, A.J.; Semenov, A.V.
Influence of temperature fluctuations on Escherichia coli O157:H7 and Salmonella enterica
serovar typhimurium in cow manure. FEMS Microb. Ecol. 2007, 60, 419428.
76. Nelson, H. The contamination of organic produce by human pathogens in animal manures.
Available online: http://eap.mcgill.ca/SFMC_1.htm (accessed on 18 December 2010).
77. Tilman, D. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology
1997, 78, 8192.
78. Girvan, M.S.; Campbell, C.D.; Killham, K.; Prosser, J.I.; Glover, L.A. Bacterial diversity
promotes community stability and functional resilience after perturbation. Environ. Microbiol.
2005, 7, 301313.
Energies 2011, 4 817

79. Semenov, A.V.; Franz, E.; van Overbeek, L.; Termorshuizen, A.J.; van Bruggen, A.H.C.
Estimating the stability of Escherichia coli O157:H7 survival in manure amended soils with
different management histories. Environ. Microbiol. 2008, 10, 14501459.
80. van der Putten, W.H.; Klironomos, J.N.; Wardle, D.A. Microbial ecology of biological invasions.
ISME J. 2007, 1, 2837.
81. Lindstrm, K.; Murwira, M.; Willems, A.; Altier, N. The biodiversity of beneficial microbe-host
mutualism: The case of rhizobia. Res. Microbiol. 2010, 161, 453463.
82. Sullivan, P. Overview of Cover Crops and Green Manures. Appropriate Technology Transfer for
Rural Areas (ATTRA). National Center for Appropriate Technology (NCAT): Fayetteville, NC,
USA, 2003. Available online: http://attra.ncat.org/attra-pub/PDF/covercrop.pdf (accessed on
12 December 2010).
83. Ding, G.; Liu, X.; Herbert, S.; Novak, J.; Amarasiriwardena, D.; Xing, B. Effect of cover crop
management on soil organic matter. Geoderma 2006, 130, 229239.
84. Knkenen, H.; Eriksson, C. Effects of undersown crops on soil mineral N and grain yield of
spring barley. Eur. J. Agron. 2007, 27, 2534.
85. Kramberger, B.; Gselman, A.; Janzekovic, M.; Kaligaric, M.; Bracko, B. Effects of cover crops on
soil mineral nitrogen and on the yield and nitrogen content of maize. Eur. J. Agron. 2009, 31,
103109.
86. Steenwerth, K.; Belina, K.M. Cover crops enhance soil organic matter, carbon dynamics and
microbiological function in an vineyard agroecosystem. Appl. Soil Ecol. 2009, 40, 359369.
87. Cherr, C.M.; Scholberg, J.M.S.; McSorley, R. Green manure approaches to crop production: A
synthesis. Agron. J. 2006, 98, 302319.
88. Hooker, K.V.; Coxon, C.E.; Hackett, R.; Kirwan, L.E.; OKeeffe, E.; Richards, K.G. Evaluation
of cover crop and reduced cultivation for reducing nitrate leaching in Ireland. J. Environ. Qual.
2008, 37, 138145.
89. Tonitto, C.; David, M.B.; Drinkwater, L.E. Replacing bare fallows with cover crops in
fertilizer-intensive cropping systems: A meta-analysis of crop yield and N-dynamics. Agric.
Ecosyst. Environ. 2006, 112, 5872.
90. Kallenbach, C.M.; Rolston, D.E.; Horwath, W.R. Cover cropping affects soil N2O and CO2
emissions differently depending on type of irrigation. Agric. Ecosyst. Environ. 2010, 137,
251260.

2011 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 license
(http://creativecommons.org/licenses/by/3.0/).