Why is the influence of soil macrofauna on soil structure onlyconsidered 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, Chinab IRD, UMR 211 BIOEMCO, Centre IRD Bondy, 32 avenue H. Varagnat, 93143 Bondy, Francec Indo-French Cell for Water Sciences (IFCWS), Department of Civil Engineering, Indian Institute of Science (IISc), 560012 Bangalore, Indiad INRA, UR1115 ‘Plantes et Systemes de production Horticoles’, Site Agroparc, 84914 Avignon cedex 09, France

1. Introduction

Soil structure regulates a large number of ecological functions,including those that control water infiltration, percolation andretention, gas exchanges, soil organic matter (SOM) and mineralnutrients dynamics, soil microbial biomass, diversity and activityand the susceptibility of soil to erosion. It is a highly dynamicsproperty of soils (Kay, 1990) subject to a large number of variablesthat can be gathered into environmental (e.g., parent material,topography and climate responsible of shrinking/swelling andfreezing/thawing processes), anthropic (e.g., land use manage-ment, mechanical disturbance of soil structure by tillage, passageof heavy machines, etc.) and biological (e.g., displacement of soilparticles and/or stabilization of soil structure by macrofauna, plantroots and microbial activities) (Dexter, 1988; Kay, 1990; Oades,1993).

Among soil macrofauna (i.e., soil invertebrates larger than2 mm), earthworms, termites and ants are considered to playimportant roles in controlling soil structure dynamic as referred torecent reviews of Blouin et al. (2013a) for earthworms, Holt andLepage (2000) and Jouquet et al. (2011) for termites, andCammeraat and Risch (2008) for ants. They are commonly namedsoil engineers (sensu the ecosystem engineer concept defined byJones et al., 1994, 1997) because of their large population andactivities in temperate and tropical ecosystems (Lavelle, 1997;Jouquet et al., 2006). Their foraging and burrowing activities, aswell as their ability, in the case of social insects, to create neststructures with specific soil properties in and on soil, largelyinfluence the physical environment in which they live andconsequently, soil structure dynamics and the correspondingregulation of soil ecological functions and ecosystem services(Lavelle et al., 2006; Birkhofer et al., 2008). Although lesswidespread, other soil macro-invertebrates can also play animportant role in regulating ecosystem functions in someenvironments (e.g., beetles larvae (Nichols et al., 2008; Brownet al., 2010; Badorreck et al., 2012) and millipedes (Toyota et al.,2006; Fujimaki et al., 2010)). However, in comparison with

Soil & Tillage Research 146 (2015) 118–124

A R T I C L E I N F O

Article history:

Received 16 December 2013

Received in revised form 29 January 2014

Accepted 30 January 2014

Keywords:

Ants

Earthworms

Ecosystem engineers

Biogenic structures

Soil structure dynamics

Termites

A B S T R A C T

These last twenty years have seen the development of an abundant literature on the influence of soil

macrofauna on soil structure. Amongst these organisms, earthworms, termites and ants are considered

to play a key role in regulating the physical, chemical and microbiological properties of soils. Due to these

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

scientists and policy makers. Despite this abundant literature, the soil engineering concept remains a

‘preach to the choir’ and bioturbation only perceived as important for soil ecologists.

We discussed in this article the main mechanisms by which soil engineers impact soil structure and

proposed to classify soil engineers with respect to their capacity to produce biostructures and modify

them. We underlined the lack of studies considering biostructure dynamics and presented recent

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.

� 2014 Elsevier B.V. All rights reserved.

* Corresponding author. Tel.: +86 25 86 88 11 98; fax: +86 25 86 88 10 00.

E-mail address: nicobottinelli86@hotmail.com (N. Bottinelli).

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http://dx.doi.org/10.1016/j.still.2014.01.007

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earthworms, termites and ants, the effects of these organismsremain largely unexplored.

The main objectives of this review article are (i) to highlight themain mechanisms by which soil engineers influence soil structureand (ii) to discuss how their activity is perceived by soil scientistsstudying the dynamic of soil structure from a review of the existingscientific literature.

2. Influence of soil macrofauna on soil structure

2.1. Critical mechanisms

Soil engineers influence soil structure through the incorpo-ration of litter in the soil. Some species feed on litter and organicresidues on the soil surface. They incorporate these organicmatters in the soil profile within soil aggregates or in coating theirgalleries. This is the case of anecic earthworms sensu Bouche(1977), and litter- and seed-feeder termites and ants (Yamadaet al., 2005; Stadler et al., 2006; Wagner and Jones, 2006; Freymannet al., 2008; Benckiser, 2010). This incorporation of fresh organicmatter in soil, which otherwise would have been degraded on soilsurface, has large consequences for soil structure because SOM isone of the key factors controlling soil porosity and soil aggregatestability and dynamic (Tisdall and Oades, 1982).

The spheres of influence or volumes of soil influenced by soilengineers are commonly named drilosphere, termitosphere andmyrmecosphere, respectively for earthworms, termites and ants(Lavelle, 1997). With respect to their capacity to produce galleries,to modify soil aggregates properties and mineral properties, threegroups of soil engineers can be differentiated (Fig. 1):

(i) The bioturbator sensu stricto. This first group corresponds toorganisms that influence soil structure through the production ofgalleries and the translocation of soil aggregates without changingtheir internal organization, at least at the short-term scale.Galleries are formed from the displacement of earthworms in soil

or the burrowing activity of social insects. They can form largenetworks and occupy a significant volume of soil in somesituations (Capowiez et al., 1998; Mando et al., 1999; Buhl et al.,2004; Perna et al., 2008). Obviously, these large macropores are ofprimary importance in the regulation of water infiltration, thediffusion of solutes (Ehlers, 1975; Nkem et al., 2000; Leonard andRajot, 2001; Cammeraat et al., 2002; Dominguez et al., 2004; Zeheet al., 2010), gas exchanges and aeration through soil (Kretzschmarand Monestiez, 1992; Capowiez et al., 2006), and they are alsoexpected to influence the spatial distribution of roots and plants(Springett and Gray, 1997; Traore et al., 2008). Some speciesprimarily modify soil porosity but their effects on soil aggregationdynamics are indeed very limited. This group is typicallyrepresented by ants that only displace soil aggregates for thecreation of their nest structure and subterranean galleries, and alsoincludes burrowing dung beetles, scarabidae and millipede species(Nichols et al., 2008; Snyder et al., 2009).

(ii) The soil aggregate re-organizers. This second group isrepresented by species that are able to modify soil structurethrough both the construction of galleries and the consumption ofsoil aggregates, called biogenic aggregates (Lavelle, 2002). Thisgroup includes most of the termite and earthworm species(Jouquet et al., 2011; Blouin et al., 2013b) but it can also includesome geophagous millipede species (Toyota et al., 2006; Fujimakiet al., 2010). This group is characterized by an ability to modify theinternal organization of soil aggregates. While the quantity of soilaggregates that have been produced by soil engineers is difficult toestimate (Jouquet et al., 2009; Bottinelli et al., 2012, 2013), severalstudies showed that earthworm casts can make up the majority ofsoil aggregates in the soil surface or even a whole soil horizon insome situations. As an example, the earthworm species Amynthas

khami accumulates a large quantity of water stable casts on the soilsurface in some environments in Northern Vietnam (from 8 to22 kg casts m�2) that forms a typical granular horizon from 5 to10 cm deep (Jouquet et al., 2008b). The same hypothesis has been

[(Fig._1)TD$FIG]

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.

N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124 119

made for termites in some tropical soils (Eschenbrenner, 1986;Jungerius et al., 1999; Reatto et al., 2009). Biogenic aggregates canbe produced after the grinding of soil particles by termitemandibles and the mixture with their saliva (in the case of thelitter-feeder termites for the production of their nests andgalleries) or they are egested in the form of faecal pellets (in thecase of earthworm casts or soil aggregates egested by soil-feedingtermites for the construction of their nests and subterraneangalleries). The modification of soil aggregates can be limited to aphysical reorganization of the elementary constituents of soilaggregates after their mixing with saliva and/or intestinal mucusthat acquire a new organization after drying. This is for examplesoil aggregates used by termites to cover the litter or used forforaging on the soil surface. These macroaggregates usually havevery similar properties than the surrounding soil (Jouquet et al.,2002a; Diouf et al., 2006) and it is therefore likely that themodification of their internal organization is also very limited, ifnot similar to that of the bulk soil. In other situations, thereorganization of soil aggregates is very important and results intotally different soil physical, chemical and biological properties.This occurs with earthworms, where the pre-existing microstruc-ture of soil aggregate is completely destroyed in the foregut (Baroiset al., 1993). Then, during gut transit, clay minerals and organicmaterials are intimately mixed and become encrusted with mucusto create a new nucleus for microaggregate formation (Shipitaloand Protz, 1989; Bossuyt et al., 2004, 2005; Pulleman et al.,2005a,b; Bossuyt et al., 2006). Within the excreted casts, dryingand ageing facilitate the strengthening of the bonds betweenorganic materials, mucus and minerals to stabilize the newlyformed microaggregates (Bossuyt et al., 2004). Earthworms canalso select and enrich soil aggregates in SOM and clay content thatcontribute to increase soil aggregate stability (Barois et al., 1999;Jouquet et al., 2008a). Another example can be given with fungus-growing termite species (Isoptera, Macrotermitinae). Thesetermite species can retrieve wet soil particles enriched in claydeep in the soil profile, even down to the water table in someoccasions, and accumulate them on the soil surface in their neststructure (Holt and Lepage, 2000; Jouquet et al., 2004b, 2011).Although unknown, it is likely that the degradation of the termitenests by the rain or any organism results in the remobilization ofthese clay particles and nutrients in the surrounding environment(Janeau and Valentin, 1987; Gosling et al., 2012), then affecting soilstructural properties.

(iii) The mineral weathering agents. Finally, this last groupcorresponds to organisms that are able to modify soil structure,from the construction of galleries, the modification of soilaggregate properties to the weathering of clay particles. Althoughlittle information is available on this topic, several studies showthat termites (Jouquet et al., 2002b, 2007) and earthworms (Suzukiet al., 2003; Carpenter et al., 2007; Liu et al., 2011) might be able tofasten the weathering of soil minerals. However, the importance ofthis alteration is probably variable and depends on both the soilproperties and the termite and earthworm species. For example,the ability of termites to modify clay mineralogy seems to belimited to fungus-growing species (Jouquet et al., 2011; Mujinyaet al., 2011). Very little information is available for earthworms andtherefore more researches are required to determine if theseabilities of termites and earthworms, to fasten the degradation ofsoil minerals are or not an exception to the rule.

2.2. More consideration should be given to the lifetime of biogenic

aggregates

The overall influence of soil engineers on soil structure result onthe balance between their ability to incorporate surface residues insoil, to produce biogenic aggregates and galleries, and the lifetime

of these structures in soil. If information is available on theproduction dynamic of earthworm casts and galleries (Lee, 1985;Capowiez, 2000; Capowiez and Belzunces, 2001; Capowiez et al.,2001, 2014; Felten and Emmerling, 2009), very few studiesmeasure the evolution of these structures in field submitted topedoclimatic or anthropic forces or from ingestion by other soilorganisms (Ligthart and Peek, 1997; Capowiez et al., 1998; LeBayon and Binet, 1999; Mariani et al., 2007; Jouquet et al., 2010a).We assume that one of the main obstacles is our difficulty todetermine the origin of soil aggregates and pores that have beenproduced by soil engineers.

In many studies the dynamics of biostructures is only discussedthrough the measurement of aggregate stability. The stability ofsoil aggregates produced by earthworms is variable. If a higher soilstructural stability is usually measured, especially when aggre-gates are enriched in SOM and/or clay content (Barois et al., 1999;Blanchart et al., 2004; Jouquet et al., 2008a), neutral (Coq et al.,2007; Bottinelli et al., 2010a) or lower structural stability have alsobeen found in some situations (Larink et al., 2001; Bottinelli et al.,2010b). Concerning termites and ants, we are clearly missinginformation on the quantity of aggregates and galleries they areable to produce over time. These are probably highly variable anddepend on the availability of food and the age of the colonies(Campora and Grace, 2004). Recent study suggests these soilaggregates are very unstable and fragment very rapidly whendeposited on the soil surface, then contributing to the slacking ofsoil aggregates and promoting the soil detachment rate and soilerosion (Jouquet et al., 2012). However, when used to producetermite or ant nests, these aggregates are likely to be very stableand to last for a very long time, from months to decades, if notcenturies to thousands of years (Picker et al., 2007; Renard et al.,2013). As a consequence, we are nowadays far from being able tomodel the influence of soil engineers on soil structure despite thedevelopment of models (Bastardie et al., 2002; Blanchart et al.,2009). This is even more obvious with social insects whichinfluence soil structure at larger spatial and temporal scales.Termite mound nests can constitute prominent features of tropicallandscapes and influence the hydrology and diversity of thevegetation and soil macro-invertebrates at the ecosystem scaleduring hundreds to thousands of years (Jouquet et al., 2004a;Picker et al., 2007; James et al., 2008; Choosai et al., 2009;Erpenbach et al., 2012; Gosling et al., 2012; Renard et al., 2013).Examples are the large abundance of ant nests that can cover 7–12% of grassland landscapes in certain environments, then creating‘antscapes’ (Boots and Clipson, 2013) and the ‘heuweltjies’ termitemounds that can occupy 14–25% of the land surface in South Africawith densities ranging from 143 to 704 mounds km�2 (Picker et al.,2007).

Basically biogenic structures are usually recognized fromsurrounding aggregates through their shape, size, colour, surfacefeatures and internal fabric. Conventional methods used toquantify soil biogenic aggregates are manual sorting (Topoliantzet al., 2000; Pulleman et al., 2005a; Velasquez et al., 2007; Jouquetet al., 2008a), point counting (Jongmans et al., 2003; Davidson andGrieve, 2006) and 2D image analysis on soil thin section and/orphotography (Hallaire et al., 2000; VandenBygaart et al., 2000;Bottinelli et al., 2010a; Lamande et al., 2011). As a result they areexperimenter dependent, laborious, destructive and finally givelimited spatial and temporal resolutions on the dynamics ofaggregation or disaggregation. However, the recent awareness ofsoil ecologists for the near infrared reflectance spectroscopy (NIRS)and X-ray computed tomography (CT) should enable betterunderstanding on the production, stabilization and degradationof these aggregates and soil pores directly in the field. NIRS hasproved to be an excellent method for separating on the one handbiogenic aggregates from their surrounding soil environment and

N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124120

on the other hand soil aggregates produced by different species(Hedde et al., 2005; Velasquez et al., 2007; Jouquet et al., 2009,2010b; Zangerle et al., 2011). More studies are now needed toexplore the actual capacity of NIRS to quantify the usefulness ofthis method in soils with contrasting biological activities aspointed out by Bottinelli et al. (2013). By its non-destructive andcomprehensive 3D character X-ray CT offers new opportunities tofollow the dynamics of soil porosity. Most of the X-ray CT analyseshave been conducted in controlled environments for characteriz-ing earthworm burrow morphology (Joschko et al., 1991; Jegouet al., 1998, 1999, 2000, 2001a,b; Capowiez et al., 2001, 2003) andtermite nest structure (Perna et al., 2008), whereas alternately fewwere carried out on undisturbed columns collected directly in thefield (Daniel et al., 1997; Capowiez et al., 1998, 2000; Jegou et al.,2002). The study of Capowiez et al. (1998) pointed out the stronginterest of this technique by following earthworm burrowsthrough two contrasted seasons. We believe that using X-ray CTwould provide valuable data concerning the lifetime of biostruc-tures in the field, as well as determining the limit of the sphere ofinfluence of soil engineers, as shown by recent studies (Schraderet al., 2007; Capowiez et al., 2011; Rogasik et al., 2014).

3. Soil macrofauna and soil sciences

3.1. Soil scientists neglect the role of soil macrofauna

From the above-mentioned literature, soil ecologists usuallyconsider that soil macrofauna, and especially soil engineer species,are key regulators of soil structure. However, how important aresoil engineers for soil scientists and in particular for physicistsseeking to measure and predict the dynamic of soil structure? Inanswer to this question, after researching in the Web of Sciencedatabase, we counted the percentage of articles published theselast five years with reference to the influence of earthworms,termites and ants on soil structure in the main journals of soilscience (Fig. 2). The percentage found is not all-inclusive because itis restricted to the articles that have ‘earthworm’, ‘termite’ or ‘ant’and ‘soil structure’ in the title or keywords, and because thismethod is restricted to only ten journals (see the list in the figurecaption) selected according to their impact factors. This excludes,for example, studies of soil macroporosity that did not mention thesoil organisms that create this macroporosity (Perret et al., 1999;Deurer et al., 2009). This approach clearly shows that the

percentage of articles dealing with the influence of earthwormson soil structure is clearly higher than those on termites and antswhich never reach more than 5% of the total quantity of articles.Although higher than with termites and ants, the percentage ofarticles dealing with earthworms and soil structure remains low. Itonly reaches between 5% and 10% of the published articles, exceptfor three journals that are all aiming at studying soil ecology(Applied Soil Ecology, Pedobiologia and European Journal of SoilBiology). Regarding the importance given by soil ecologists to theimpact of earthworms, termites and ants on soil structure, theseresults are therefore somewhat surprising and show the differentapproaches and interests between soil physicists and soilecologists. Another example of this low interest of soil scientistsfor soil macrofauna activity (or low interest of soil ecologists forsoil physical processes) is stressed with the very low quantity oforal and poster communications in the International Union of SoilScience (IUSS) congress held in Brisbane in 2010. Indeed, athorough examination revealed only 2, 1 and 0 oral communica-tions and 2, 0 and 2 poster presentations, respectively forearthworms, termites and ants, for a total number of 360 and957 oral and poster communications, respectively. The samestatement will probably be done for the next IUSS congress to beheld in Jeju, Korea. In the posted programme (http://www.20wcss.org/sub03_1.php), it is indeed worth highlightingthat the soil biology symposium only focuses on soil microorgan-isms and that the soil macrofauna is not even mentioned.

3.2. Main reasons

Several hypotheses are suggested to explain this lack ofconsideration for soil macrofauna, and earthworms, termitesand ants in particular by soil scientists working on soil structure:

First, conventional agriculture, based on large inputs ofpesticides and classical tillage, has a dramatic influence on soilmacrofauna (Beare et al., 1997; Jones et al., 2003; Van Capelle et al.,2012; Ponge et al., 2013). It is therefore not surprising that researchprojects on soil structure in agricultural systems do not considerthe influence of organisms that are not observed at high densities.However, it is likely that the development of research in bothconservation agriculture and organic farming will reverse thistrend in the near future since the abundance and diversity ofmacrofauna are usually higher in the above-mentioned environ-

[(Fig._2)TD$FIG]

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

of Science in selected journals in soil science and biology with high impact factors

(Applied Soil Ecology, Biology and Fertility of Soils, European Journal of Soil Biology,

European Journal of Soil Science, Geoderma, Pedobiologia, Soil Biology and

Biochemistry and Soil Tillage Research). Numbers above histograms are total

number of articles referenced in Web of Science in September 2013 with the topic

‘soil structure’ these last five years.

[(Fig._3)TD$FIG]

Fig. 3. Schematic representation of the relation between land use intensity and soil

biodiversity. While conventional agriculture is usually considered to negatively

influence soil biodiversity, natural systems (fallow, pasture and forest) are

associated with high soil fauna activity and diversity. Conservation agriculture

(no tillage, agroforestry, etc.) relies on the development of biodiversity in soil for the

promotion of essential ecological processes such as those controlling water

infiltration and retention, soil organic matter protection, and so on.

N. Bottinelli et al. / Soil & Tillage Research 146 (2015) 118–124 121

ments (Hole et al., 2005; Scopel et al., 2013) (Fig. 3). In arable lands,the development of reduced tillage, will for example be positive forearthworm abundance, especially anecic ones (Chan, 2001;Capowiez et al., 2009) and additionally will highlight the variousecosystem services these organisms can provide such as theregeneration of compacted soils (Capowiez et al., 2012).

Second, soil structure is under the control of both abiotic andbiotic driving factors and their respective importance varyaccording to a large set of environmental variables. The potentialeffect of soil engineers on soil structure could be over sighted whenthe action of other factors like soil shrinking-swelling, freezing-thawing, tillage or roots growth are dominant (Oades, 1993;Drewry, 2006). However, it remains that more information isneeded to determine when and where soil engineers are playing asignificant role in soil functioning.

Third, Blouin et al. (2013b) mentioned a ‘balkanization’ of theresearch in the field of ecological engineering and the need to crossthe frontiers between fields and disciplines. We assume that thestudy of the influence of soil macrofauna on soil structure is facingthe same challenge. Ecology is the science that studies the interactionbetween organisms and other organisms and their interaction withtheir environment. In soil, an abundant number of researches havefocused on the inventory of soil invertebrate diversity, the structureof this diversity and its response to land use change or agriculturalpractices. This approach has mainly been carried out by soilbiologists. However, the possibility that soil invertebrates alsomodify their environment and that a feedback exists between theecology of soil engineers and the physical properties of theirenvironment is relatively recent. It emerged in the beginning of the90s, and especially after the publication of Jones et al. (1994, 1997)and the definition of the ‘ecosystem engineer’ concept. This newapproach requires the collaboration of soil ecologists and physicists.

Finally, another reason might result from the fact that fornumerous soil ecologists the effects of soil macrofauna on soilstructure are solely related to their own abundance or diversity(Pulleman et al., 2012). Obviously, this relation is simplistic and donot consider the activities of soil organisms, the properties anddynamics of biostructures. As an example, Jouquet et al. (2012)showed that soil engineers might in some situations play a moreimportant role through the aggregates they produce than theirown abundance or diversity. As a result, we consider that the jointstudy of soil physics and soil ecology are necessary to combine for amore accurate knowledge in this research topic.

4. Main challenges and major questions that need to beanswered

This review shows that more research is needed on the influenceof soil engineers on soil structure dynamic, and this is obviouslymore the case for social insects than for earthworms. The definitionof ecosystem engineering relies on the ability of organisms to modifytheir physical environment, and then the habitat for other organisms(Jones et al., 1994, 1997). An abundance of literature is available onthe influence of soil engineers on soil microbial communities andactivity, SOM dynamic and nutrient cycling, or plant growth.However, this influence mainly results from the impact of soilengineers on soil structure and it is surprising to realize that thislatter aspect has been clearly neglected. We assume that thedetermination of (i) the quantity of biopores and biogenic aggregatesthat soil engineers are able to produce, (ii) the distribution of thesestructures at the plot and landscape scales, (iii) and the lifetime ofthese structures are some of the major questions which need to beanswered to develop a more complete understanding of theinfluence of soil engineers on soil structure dynamic. We assumethat these questions can be answered only if soil ecologists work incollaboration with soil physicists. In this context, the development

of technologies such as NIRS and X-ray CT could be of great interests.These technologies could allow soil ecologists to better answer to theabove-mentioned questions as well as to understand the linkbetween the influence of soil engineers on soil aggregation and soilporosity and the resistance of soils to perturbations (compaction,temporary flooding, etc.). These technologies could be also of greathelp to determine the limit of the sphere of influence of soilengineers. This review also shows that more work has to be carriedout in order to define when and where soil engineers are playing avital role in soil structure dynamics. This question has largeimplications in terms of soil restoration and ecological engineering(Blouin et al., 2013a; Jouquet et al., 2014) and we consider that itmust be the preliminary step before any decision to restore soilengineers population in soil, especially in degraded agriculturallands.

Acknowledgments

As in any review, the concepts and ideas formulated in thisarticle result from dialogues with many colleagues and peers, whoare all acknowledged. We are also grateful to Dexin Zhang for herillustrations and Michelle Van Deventer for useful Englishcorrections on the manuscript. This work was supported finan-cially by the Natural Science Foundation of China (code:41250110526), the Chinese Academy of Sciences Fellowships forYoung International Scientists (code: 2012Y1ZB003) and theFrench Embassy from China. Dr. Xinhua Peng gratefully thanksthe ’100 Talents Program’ of the Chinese Academy of Sciences.

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