Soil & Tillage Research 146 (2015) 118–124

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Soil & Tillage Research

journal homepage: www.elsevier.com/locate/still

Why is the influence of soil macrofauna on soil structure only

considered by soil ecologists?
N. Bottinelli a,*, P. Jouquet b,c, Y. Capowiez d, P. Podwojewski b, M. Grimaldi b, X. Peng a
a
State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, CAS, Nanjing 210008, China
b
IRD, UMR 211 BIOEMCO, Centre IRD Bondy, 32 avenue H. Varagnat, 93143 Bondy, France
c
Indo-French Cell for Water Sciences (IFCWS), Department of Civil Engineering, Indian Institute of Science (IISc), 560012 Bangalore, India
d
INRA, UR1115 ‘Plantes et Systèmes de production Horticoles’, Site Agroparc, 84914 Avignon cedex 09, France

A R T I C L E I N F O A B S T R A C T

Article history: These last twenty years have seen the development of an abundant literature on the influence of soil
Received 16 December 2013 macrofauna on soil structure. Amongst these organisms, earthworms, termites and ants are considered
Received in revised form 29 January 2014 to play a key role in regulating the physical, chemical and microbiological properties of soils. Due to these
Accepted 30 January 2014
influential impacts, soil ecologists consider these soil macro-invertebrates as ‘soil engineers’ and their
diversity and abundance are nowadays considered as relevant bioindicators of soil quality by many
Keywords: scientists and policy makers. Despite this abundant literature, the soil engineering concept remains a
Ants
‘preach to the choir’ and bioturbation only perceived as important for soil ecologists.
Earthworms
We discussed in this article the main mechanisms by which soil engineers impact soil structure and
Ecosystem engineers
Biogenic structures proposed to classify soil engineers with respect to their capacity to produce biostructures and modify
Soil structure dynamics them. We underlined the lack of studies considering biostructure dynamics and presented recent
Termites techniques in this purpose. We discussed why soil engineering concept is mainly considered by soil
ecologists and call for a better collaboration between soil ecologists and soil physicists. Finally, we
summarized main challenges and questions that need to be answered to integrate soil engineers
activities in soil structure studies.
ß 2014 Elsevier B.V. All rights reserved.

1. Introduction Among soil macrofauna (i.e., soil invertebrates larger than

2 mm), earthworms, termites and ants are considered to play
Soil structure regulates a large number of ecological functions, important roles in controlling soil structure dynamic as referred to
including those that control water infiltration, percolation and recent reviews of Blouin et al. (2013a) for earthworms, Holt and
retention, gas exchanges, soil organic matter (SOM) and mineral Lepage (2000) and Jouquet et al. (2011) for termites, and
nutrients dynamics, soil microbial biomass, diversity and activity Cammeraat and Risch (2008) for ants. They are commonly named
and the susceptibility of soil to erosion. It is a highly dynamics soil engineers (sensu the ecosystem engineer concept defined by
property of soils (Kay, 1990) subject to a large number of variables Jones et al., 1994, 1997) because of their large population and
that can be gathered into environmental (e.g., parent material, activities in temperate and tropical ecosystems (Lavelle, 1997;
topography and climate responsible of shrinking/swelling and Jouquet et al., 2006). Their foraging and burrowing activities, as
freezing/thawing processes), anthropic (e.g., land use manage- well as their ability, in the case of social insects, to create nest
ment, mechanical disturbance of soil structure by tillage, passage structures with specific soil properties in and on soil, largely
of heavy machines, etc.) and biological (e.g., displacement of soil influence the physical environment in which they live and
particles and/or stabilization of soil structure by macrofauna, plant consequently, soil structure dynamics and the corresponding
roots and microbial activities) (Dexter, 1988; Kay, 1990; Oades, regulation of soil ecological functions and ecosystem services
1993). (Lavelle et al., 2006; Birkhofer et al., 2008). Although less
widespread, other soil macro-invertebrates can also play an
important role in regulating ecosystem functions in some
environments (e.g., beetles larvae (Nichols et al., 2008; Brown
* Corresponding author. Tel.: +86 25 86 88 11 98; fax: +86 25 86 88 10 00.
et al., 2010; Badorreck et al., 2012) and millipedes (Toyota et al.,
E-mail address: [email protected] (N. Bottinelli). 2006; Fujimaki et al., 2010)). However, in comparison with

http://dx.doi.org/10.1016/j.still.2014.01.007
0167-1987/ß 2014 Elsevier B.V. All rights reserved.
 N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124 119

earthworms, termites and ants, the effects of these organisms or the burrowing activity of social insects. They can form large
remain largely unexplored. networks and occupy a significant volume of soil in some
The main objectives of this review article are (i) to highlight the situations (Capowiez et al., 1998; Mando et al., 1999; Buhl et al.,
main mechanisms by which soil engineers influence soil structure 2004; Perna et al., 2008). Obviously, these large macropores are of
and (ii) to discuss how their activity is perceived by soil scientists primary importance in the regulation of water infiltration, the
studying the dynamic of soil structure from a review of the existing diffusion of solutes (Ehlers, 1975; Nkem et al., 2000; Léonard and
scientific literature. Rajot, 2001; Cammeraat et al., 2002; Dominguez et al., 2004; Zehe
et al., 2010), gas exchanges and aeration through soil (Kretzschmar
2. Influence of soil macrofauna on soil structure and Monestiez, 1992; Capowiez et al., 2006), and they are also
expected to influence the spatial distribution of roots and plants
2.1. Critical mechanisms (Springett and Gray, 1997; Traore et al., 2008). Some species
primarily modify soil porosity but their effects on soil aggregation
Soil engineers influence soil structure through the incorpo- dynamics are indeed very limited. This group is typically
ration of litter in the soil. Some species feed on litter and organic represented by ants that only displace soil aggregates for the
residues on the soil surface. They incorporate these organic creation of their nest structure and subterranean galleries, and also
matters in the soil profile within soil aggregates or in coating their includes burrowing dung beetles, scarabidae and millipede species
galleries. This is the case of anecic earthworms sensu Bouché (Nichols et al., 2008; Snyder et al., 2009).
(1977), and litter- and seed-feeder termites and ants (Yamada (ii) The soil aggregate re-organizers. This second group is
et al., 2005; Stadler et al., 2006; Wagner and Jones, 2006; Freymann represented by species that are able to modify soil structure
et al., 2008; Benckiser, 2010). This incorporation of fresh organic through both the construction of galleries and the consumption of
matter in soil, which otherwise would have been degraded on soil soil aggregates, called biogenic aggregates (Lavelle, 2002). This
surface, has large consequences for soil structure because SOM is group includes most of the termite and earthworm species
one of the key factors controlling soil porosity and soil aggregate (Jouquet et al., 2011; Blouin et al., 2013b) but it can also include
stability and dynamic (Tisdall and Oades, 1982). some geophagous millipede species (Toyota et al., 2006; Fujimaki
The spheres of influence or volumes of soil influenced by soil et al., 2010). This group is characterized by an ability to modify the
engineers are commonly named drilosphere, termitosphere and internal organization of soil aggregates. While the quantity of soil
myrmecosphere, respectively for earthworms, termites and ants aggregates that have been produced by soil engineers is difficult to
(Lavelle, 1997). With respect to their capacity to produce galleries, estimate (Jouquet et al., 2009; Bottinelli et al., 2012, 2013), several
to modify soil aggregates properties and mineral properties, three studies showed that earthworm casts can make up the majority of
groups of soil engineers can be differentiated (Fig. 1): soil aggregates in the soil surface or even a whole soil horizon in
(i) The bioturbator sensu stricto. This first group corresponds to some situations. As an example, the earthworm species Amynthas
organisms that influence soil structure through the production of khami accumulates a large quantity of water stable casts on the soil
galleries and the translocation of soil aggregates without changing surface in some environments in Northern Vietnam (from 8 to
their internal organization, at least at the short-term scale. 22 kg casts m 2) that forms a typical granular horizon from 5 to
[(Fig._1)TD$IG]Galleries are formed from the displacement of earthworms in soil 10 cm deep (Jouquet et al., 2008b). The same hypothesis has been

Fig. 1. How soil engineers influence soil structure is variable, with respect to their capacity to produce galleries, modify soil aggregates and mineral properties. Three groups
can be differentiated: (i) the bioturbator sensu stricto, (ii) the soil aggregate re-organizers and (iii) the mineral weathering agents.
120 N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124

made for termites in some tropical soils (Eschenbrenner, 1986; of these structures in soil. If information is available on the
Jungerius et al., 1999; Reatto et al., 2009). Biogenic aggregates can production dynamic of earthworm casts and galleries (Lee, 1985;
be produced after the grinding of soil particles by termite Capowiez, 2000; Capowiez and Belzunces, 2001; Capowiez et al.,
mandibles and the mixture with their saliva (in the case of the 2001, 2014; Felten and Emmerling, 2009), very few studies
litter-feeder termites for the production of their nests and measure the evolution of these structures in field submitted to
galleries) or they are egested in the form of faecal pellets (in the pedoclimatic or anthropic forces or from ingestion by other soil
case of earthworm casts or soil aggregates egested by soil-feeding organisms (Ligthart and Peek, 1997; Capowiez et al., 1998; Le
termites for the construction of their nests and subterranean Bayon and Binet, 1999; Mariani et al., 2007; Jouquet et al., 2010a).
galleries). The modification of soil aggregates can be limited to a We assume that one of the main obstacles is our difficulty to
physical reorganization of the elementary constituents of soil determine the origin of soil aggregates and pores that have been
aggregates after their mixing with saliva and/or intestinal mucus produced by soil engineers.
that acquire a new organization after drying. This is for example In many studies the dynamics of biostructures is only discussed
soil aggregates used by termites to cover the litter or used for through the measurement of aggregate stability. The stability of
foraging on the soil surface. These macroaggregates usually have soil aggregates produced by earthworms is variable. If a higher soil
very similar properties than the surrounding soil (Jouquet et al., structural stability is usually measured, especially when aggre-
2002a; Diouf et al., 2006) and it is therefore likely that the gates are enriched in SOM and/or clay content (Barois et al., 1999;
modification of their internal organization is also very limited, if Blanchart et al., 2004; Jouquet et al., 2008a), neutral (Coq et al.,
not similar to that of the bulk soil. In other situations, the 2007; Bottinelli et al., 2010a) or lower structural stability have also
reorganization of soil aggregates is very important and results in been found in some situations (Larink et al., 2001; Bottinelli et al.,
totally different soil physical, chemical and biological properties. 2010b). Concerning termites and ants, we are clearly missing
This occurs with earthworms, where the pre-existing microstruc- information on the quantity of aggregates and galleries they are
ture of soil aggregate is completely destroyed in the foregut (Barois able to produce over time. These are probably highly variable and
et al., 1993). Then, during gut transit, clay minerals and organic depend on the availability of food and the age of the colonies
materials are intimately mixed and become encrusted with mucus (Campora and Grace, 2004). Recent study suggests these soil
to create a new nucleus for microaggregate formation (Shipitalo aggregates are very unstable and fragment very rapidly when
and Protz, 1989; Bossuyt et al., 2004, 2005; Pulleman et al., deposited on the soil surface, then contributing to the slacking of
2005a,b; Bossuyt et al., 2006). Within the excreted casts, drying soil aggregates and promoting the soil detachment rate and soil
and ageing facilitate the strengthening of the bonds between erosion (Jouquet et al., 2012). However, when used to produce
organic materials, mucus and minerals to stabilize the newly termite or ant nests, these aggregates are likely to be very stable
formed microaggregates (Bossuyt et al., 2004). Earthworms can and to last for a very long time, from months to decades, if not
also select and enrich soil aggregates in SOM and clay content that centuries to thousands of years (Picker et al., 2007; Renard et al.,
contribute to increase soil aggregate stability (Barois et al., 1999; 2013). As a consequence, we are nowadays far from being able to
Jouquet et al., 2008a). Another example can be given with fungus- model the influence of soil engineers on soil structure despite the
growing termite species (Isoptera, Macrotermitinae). These development of models (Bastardie et al., 2002; Blanchart et al.,
termite species can retrieve wet soil particles enriched in clay 2009). This is even more obvious with social insects which
deep in the soil profile, even down to the water table in some influence soil structure at larger spatial and temporal scales.
occasions, and accumulate them on the soil surface in their nest Termite mound nests can constitute prominent features of tropical
structure (Holt and Lepage, 2000; Jouquet et al., 2004b, 2011). landscapes and influence the hydrology and diversity of the
Although unknown, it is likely that the degradation of the termite vegetation and soil macro-invertebrates at the ecosystem scale
nests by the rain or any organism results in the remobilization of during hundreds to thousands of years (Jouquet et al., 2004a;
these clay particles and nutrients in the surrounding environment Picker et al., 2007; James et al., 2008; Choosai et al., 2009;
(Janeau and Valentin, 1987; Gosling et al., 2012), then affecting soil Erpenbach et al., 2012; Gosling et al., 2012; Renard et al., 2013).
structural properties. Examples are the large abundance of ant nests that can cover 7–
(iii) The mineral weathering agents. Finally, this last group 12% of grassland landscapes in certain environments, then creating
corresponds to organisms that are able to modify soil structure, ‘antscapes’ (Boots and Clipson, 2013) and the ‘heuweltjies’ termite
from the construction of galleries, the modification of soil mounds that can occupy 14–25% of the land surface in South Africa
aggregate properties to the weathering of clay particles. Although with densities ranging from 143 to 704 mounds km 2 (Picker et al.,
little information is available on this topic, several studies show 2007).
that termites (Jouquet et al., 2002b, 2007) and earthworms (Suzuki Basically biogenic structures are usually recognized from
et al., 2003; Carpenter et al., 2007; Liu et al., 2011) might be able to surrounding aggregates through their shape, size, colour, surface
fasten the weathering of soil minerals. However, the importance of features and internal fabric. Conventional methods used to
this alteration is probably variable and depends on both the soil quantify soil biogenic aggregates are manual sorting (Topoliantz
properties and the termite and earthworm species. For example, et al., 2000; Pulleman et al., 2005a; Velasquez et al., 2007; Jouquet
the ability of termites to modify clay mineralogy seems to be et al., 2008a), point counting (Jongmans et al., 2003; Davidson and
limited to fungus-growing species (Jouquet et al., 2011; Mujinya Grieve, 2006) and 2D image analysis on soil thin section and/or
et al., 2011). Very little information is available for earthworms and photography (Hallaire et al., 2000; VandenBygaart et al., 2000;
therefore more researches are required to determine if these Bottinelli et al., 2010a; Lamandé et al., 2011). As a result they are
abilities of termites and earthworms, to fasten the degradation of experimenter dependent, laborious, destructive and finally give
soil minerals are or not an exception to the rule. limited spatial and temporal resolutions on the dynamics of
aggregation or disaggregation. However, the recent awareness of
2.2. More consideration should be given to the lifetime of biogenic soil ecologists for the near infrared reflectance spectroscopy (NIRS)
aggregates and X-ray computed tomography (CT) should enable better
understanding on the production, stabilization and degradation
The overall influence of soil engineers on soil structure result on of these aggregates and soil pores directly in the field. NIRS has
the balance between their ability to incorporate surface residues in proved to be an excellent method for separating on the one hand
soil, to produce biogenic aggregates and galleries, and the lifetime biogenic aggregates from their surrounding soil environment and
 N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124 121

on the other hand soil aggregates produced by different species percentage of articles dealing with the influence of earthworms
(Hedde et al., 2005; Velasquez et al., 2007; Jouquet et al., 2009, on soil structure is clearly higher than those on termites and ants
2010b; Zangerlé et al., 2011). More studies are now needed to which never reach more than 5% of the total quantity of articles.
explore the actual capacity of NIRS to quantify the usefulness of Although higher than with termites and ants, the percentage of
this method in soils with contrasting biological activities as articles dealing with earthworms and soil structure remains low. It
pointed out by Bottinelli et al. (2013). By its non-destructive and only reaches between 5% and 10% of the published articles, except
comprehensive 3D character X-ray CT offers new opportunities to for three journals that are all aiming at studying soil ecology
follow the dynamics of soil porosity. Most of the X-ray CT analyses (Applied Soil Ecology, Pedobiologia and European Journal of Soil
have been conducted in controlled environments for characteriz- Biology). Regarding the importance given by soil ecologists to the
ing earthworm burrow morphology (Joschko et al., 1991; Jégou impact of earthworms, termites and ants on soil structure, these
et al., 1998, 1999, 2000, 2001a,b; Capowiez et al., 2001, 2003) and results are therefore somewhat surprising and show the different
termite nest structure (Perna et al., 2008), whereas alternately few approaches and interests between soil physicists and soil
were carried out on undisturbed columns collected directly in the ecologists. Another example of this low interest of soil scientists
field (Daniel et al., 1997; Capowiez et al., 1998, 2000; Jégou et al., for soil macrofauna activity (or low interest of soil ecologists for
2002). The study of Capowiez et al. (1998) pointed out the strong soil physical processes) is stressed with the very low quantity of
interest of this technique by following earthworm burrows oral and poster communications in the International Union of Soil
through two contrasted seasons. We believe that using X-ray CT Science (IUSS) congress held in Brisbane in 2010. Indeed, a
would provide valuable data concerning the lifetime of biostruc- thorough examination revealed only 2, 1 and 0 oral communica-
tures in the field, as well as determining the limit of the sphere of tions and 2, 0 and 2 poster presentations, respectively for
influence of soil engineers, as shown by recent studies (Schrader earthworms, termites and ants, for a total number of 360 and
et al., 2007; Capowiez et al., 2011; Rogasik et al., 2014). 957 oral and poster communications, respectively. The same
statement will probably be done for the next IUSS congress to be
3. Soil macrofauna and soil sciences held in Jeju, Korea. In the posted programme (http://
www.20wcss.org/sub03_1.php), it is indeed worth highlighting
3.1. Soil scientists neglect the role of soil macrofauna that the soil biology symposium only focuses on soil microorgan-
isms and that the soil macrofauna is not even mentioned.
From the above-mentioned literature, soil ecologists usually
consider that soil macrofauna, and especially soil engineer species, 3.2. Main reasons
are key regulators of soil structure. However, how important are
soil engineers for soil scientists and in particular for physicists Several hypotheses are suggested to explain this lack of
seeking to measure and predict the dynamic of soil structure? In consideration for soil macrofauna, and earthworms, termites
answer to this question, after researching in the Web of Science and ants in particular by soil scientists working on soil structure:
database, we counted the percentage of articles published these First, conventional agriculture, based on large inputs of
last five years with reference to the influence of earthworms, pesticides and classical tillage, has a dramatic influence on soil
termites and ants on soil structure in the main journals of soil macrofauna (Beare et al., 1997; Jones et al., 2003; Van Capelle et al.,
science (Fig. 2). The percentage found is not all-inclusive because it 2012; Ponge et al., 2013). It is therefore not surprising that research
is restricted to the articles that have ‘earthworm’, ‘termite’ or ‘ant’ projects on soil structure in agricultural systems do not consider
and ‘soil structure’ in the title or keywords, and because this the influence of organisms that are not observed at high densities.
method is restricted to only ten journals (see the list in the figure However, it is likely that the development of research in both
caption) selected according to their impact factors. This excludes, conservation agriculture and organic farming will reverse this
for example, studies of soil macroporosity that did not mention the trend in the near future since the abundance and diversity of
soil organisms that create this macroporosity (Perret et al., 1999; [(Fig._3)TD$IG]
macrofauna are usually higher in the above-mentioned environ-
Deurer et al., 2009). This approach clearly shows that the
[(Fig._2)TD$IG]

Fig. 2. Percentage of articles containing the following keywords ‘soil structure’ and
either ‘earthworms’ (in white), ‘termites’ (in grey) or ‘ants’ (in black) in the title or in
the abstract, which were published in the previous five years and referenced in Web Fig. 3. Schematic representation of the relation between land use intensity and soil
of Science in selected journals in soil science and biology with high impact factors biodiversity. While conventional agriculture is usually considered to negatively
(Applied Soil Ecology, Biology and Fertility of Soils, European Journal of Soil Biology, influence soil biodiversity, natural systems (fallow, pasture and forest) are
European Journal of Soil Science, Geoderma, Pedobiologia, Soil Biology and associated with high soil fauna activity and diversity. Conservation agriculture
Biochemistry and Soil Tillage Research). Numbers above histograms are total (no tillage, agroforestry, etc.) relies on the development of biodiversity in soil for the
number of articles referenced in Web of Science in September 2013 with the topic promotion of essential ecological processes such as those controlling water
‘soil structure’ these last five years. infiltration and retention, soil organic matter protection, and so on.
122 N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124

ments (Hole et al., 2005; Scopel et al., 2013) (Fig. 3). In arable lands, of technologies such as NIRS and X-ray CT could be of great interests.
the development of reduced tillage, will for example be positive for These technologies could allow soil ecologists to better answer to the
earthworm abundance, especially anecic ones (Chan, 2001; above-mentioned questions as well as to understand the link
Capowiez et al., 2009) and additionally will highlight the various between the influence of soil engineers on soil aggregation and soil
ecosystem services these organisms can provide such as the porosity and the resistance of soils to perturbations (compaction,
regeneration of compacted soils (Capowiez et al., 2012). temporary flooding, etc.). These technologies could be also of great
Second, soil structure is under the control of both abiotic and help to determine the limit of the sphere of influence of soil
biotic driving factors and their respective importance vary engineers. This review also shows that more work has to be carried
according to a large set of environmental variables. The potential out in order to define when and where soil engineers are playing a
effect of soil engineers on soil structure could be over sighted when vital role in soil structure dynamics. This question has large
the action of other factors like soil shrinking-swelling, freezing- implications in terms of soil restoration and ecological engineering
thawing, tillage or roots growth are dominant (Oades, 1993; (Blouin et al., 2013a; Jouquet et al., 2014) and we consider that it
Drewry, 2006). However, it remains that more information is must be the preliminary step before any decision to restore soil
needed to determine when and where soil engineers are playing a engineers population in soil, especially in degraded agricultural
significant role in soil functioning. lands.
Third, Blouin et al. (2013b) mentioned a ‘balkanization’ of the
research in the field of ecological engineering and the need to cross Acknowledgments
the frontiers between fields and disciplines. We assume that the
study of the influence of soil macrofauna on soil structure is facing As in any review, the concepts and ideas formulated in this
the same challenge. Ecology is the science that studies the interaction article result from dialogues with many colleagues and peers, who
between organisms and other organisms and their interaction with are all acknowledged. We are also grateful to Dexin Zhang for her
their environment. In soil, an abundant number of researches have illustrations and Michelle Van Deventer for useful English
focused on the inventory of soil invertebrate diversity, the structure corrections on the manuscript. This work was supported finan-
of this diversity and its response to land use change or agricultural cially by the Natural Science Foundation of China (code:
practices. This approach has mainly been carried out by soil 41250110526), the Chinese Academy of Sciences Fellowships for
biologists. However, the possibility that soil invertebrates also Young International Scientists (code: 2012Y1ZB003) and the
modify their environment and that a feedback exists between the French Embassy from China. Dr. Xinhua Peng gratefully thanks
ecology of soil engineers and the physical properties of their the ’100 Talents Program’ of the Chinese Academy of Sciences.
environment is relatively recent. It emerged in the beginning of the
90s, and especially after the publication of Jones et al. (1994, 1997)
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