R

Ue

Pa

b

c

a

ARRA

KEVISSR

C

1

a(tuga

0h

Applied Soil Ecology 73 (2014) 34– 40

Contents lists available at ScienceDirect

Applied Soil Ecology

journa l h om epa ge: www.elsev ier .com/ locate /apsoi l

eview

tilization of earthworms and termites for the restoration ofcosystem functioning

ascal Jouqueta,∗, Eric Blanchartb, Yvan Capowiezc

IRD, UMR 211 BIOEMCO, Centre IRD Bondy, 32 Avenue H. Varagnat, 93143 Bondy, FranceIRD, UMR 210 Eco&Sols, 2 Place Viala, 34060 Montpellier, FranceINRA, UR 1115 Plantes et Systèmes Horticoles, Domaine Saint Paul, 84914 Avignon Cedex 09, France

r t i c l e i n f o

rticle history:eceived 21 May 2013eceived in revised form 17 July 2013ccepted 9 August 2013

a b s t r a c t

Soil engineers, such as earthworms and termites, are key organisms in soil functioning. They are involvedin many ecological processes and play a central role in numerous ecosystem services. This review dis-cusses the management of earthworm and termite activity for the restoration of ecosystems. We reviewmethods to promote soil engineer activity either directly through field inoculation or stimulation orindirectly through the utilization of vermicompost. Examples of their use for the restoration of acid,

eywords:cological engineeringermicompost

noculationoil

compacted or crusted, polluted, and eroded soils are also discussed. Finally, we summarize the majorobstacles hampering the utilization of soil engineer activity for the restoration of ecosystems, considernew research topics that need further development and highlight the need to consider the interactionsbetween the functions and services influenced by soil engineers.

timulationestoration

© 2013 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342. A functional classification of ecosystem engineers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 353. Methods to promote soil engineer activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354. Ecosystem restoration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375. Service of food provisioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

5.1. Acid soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375.2. Compacted and crusted soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

6. Control of erosion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 377. Detoxification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 388. Towards more intensive soil restoration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

. Introduction

Human societies derive many essential environmental goodsnd services from ecosystems, i.e. the so called ecosystem servicesCostanza et al., 1997; de Groot et al., 2002). These services include

transformations, (ii) nutrient cycling, (iii) soil structure and main-tenance, and (iv) biological population regulation. A substantialbody of literature suggests that these four functions are mainly, butnot exclusively, under the regulation of soil biodiversity (Lavelleet al., 2006; Barrios, 2007; Bullock et al., 2011).

Soil organisms regulate key biogeochemical cycles (see Lavelle

he natural processes that support the production of food, the reg-lation of water quantity and quality, the emission of greenhouseases. Following Kibblewhite et al. (2008) ecosystems servicesre under the regulation of four key ecosystem functions: (i) C

∗ Corresponding author. Tel./fax +33 (0)1 48 02 55 34.E-mail address: pascal.jouquet@ird.fr (P. Jouquet).

929-1393/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.apsoil.2013.08.004

et al., 2006; Barrios, 2007 for reviews on this subject). Among soilinvertebrates, soil engineers (sensu Lavelle et al., 1997; Jouquetet al., 2006) appear to play a more prominent role. Earthwormsand termites are the major and most studied soil engineers, due to

their dominant abundance and biomass in temperate and tropicalsoils. However, although less widespread than these two taxa, otherorganisms can also play important role in regulating ecosystemfunctions in some environments (i.e., dung beetles, Brown et al.,

P. Jouquet et al. / Applied Soil

1

10

100

100 0

100 00

Termites Earthworms Plants

5/20

16/85

6358N

umbe

rof a

r�cl

es

Topics

Fig. 1. Comparison between the number of articles referenced in Web of Sciencewith the following keywords ‘soils’; ‘restoration’ and either ‘termites’; ‘earthworms’;or ‘plants’. In total; 20 articles have been published with termites; 85 with earth-wts

22eaabstwgtttJtS

sapmrcaaw(tseqrwi‘bWnao

orms and 6358 with plants. However; a thorough examination of the articles revealhat the influence of soil engineers on the restoration of soil quality has only beentudied in 5 and 16 articles (in grey); respectively for termites and earthworms.

010; scarabeidae larvae, Rabary et al., 2008; ants, Majer et al.,007; Evans et al., 2011; millipedes, Toyota et al., 2006) but theirffects as ecosystem engineers remain unexplored. In addition tocting as detritivores, earthworms and termites modify resourcevailability to other species through the creation of biopores andiogenic aggregates. They are involved in most key soil functions,uch as the decomposition of organic residues at the soil surface,he regulation of soil organic matter turnover, nutrient cycling,ater infiltration and storage in the soil, soil erosion, and plant

rowth (Lavelle and Spain, 2001). Consequently, it is consideredhat soil engineers are an essential component of soil quality andheir abundance and diversity have been proposed as bioindica-ors of ecosystem health (Muys and Granval, 1987; Paoletti, 1999;ones et al., 2003; Ruiz et al., 2011) or to assess the level of ecosys-em restoration (Dunger and Voigtländer, 2005; Majer et al., 2007;nyder and Hendrix, 2008).

Several articles have been published in the last 20 years on theignificant influence of soil engineers on key ecological functionsnd as a consequence on the regulation of soil bio-physicochemicalroperties (see the recent reviews of Jouquet et al., 2011a for ter-ites, and Blouin et al., 2013 for earthworms). The increasing

ecognition of their importance in the regulation of key biogeo-hemical cycles has led to the suggestion that soil engineeringctivity could be developed as a cornerstone for the provision ofgricultural and non-agricultural services, such as erosion control,ater quality and supply, pollutant attenuation and degradation

De Goede and Brussaard, 2002). However, much less has been writ-en on the possibility to use the ecological functions performed byoil engineers for the restoration of ecosystem services in degradedcosystems (Curry, 2004; Eijsackers, 2011). Fig. 1 illustrates theuantity of articles published on the topic of soil restoration andeferenced in Web of Science with the utilization of termites, earth-orms and plants. Although this list is not exhaustive because

t is restricted to articles that have ‘soils’, ‘restoration’ and eithertermites’, ‘earthworms’, or ‘plants’ in the title or keywords, andecause this method may miss relevant papers not available in

eb of Science, it clearly shows how the utilization of soil engi-

eers, earthworms and termites, has been under-explored in thepproach of restoration by comparison with the classical approachf plant utilization. A review of recent studies using earthworms

Ecology 73 (2014) 34– 40 35

and termites to restore degraded ecosystems is therefore nowappropriate.

In this paper, we first review the key ecological functions per-formed by soil engineers. We then stress the methods developed topromote their activity, and identify the obstacles hampering furtherresearch on this topic. Next, we give examples of the utilization ofearthworm and termite activity for the rehabilitation of soil qualityand functioning. Finally, we summarize the major obstacles ham-pering the utilization of soil engineer activity for the restorationof ecosystems and consider new research topics that should allowthe development of sustainable practices for the rehabilitation ofdegraded ecosystems.

2. A functional classification of ecosystem engineers

The utilization of ecosystem engineers for the restoration ofecosystem services is supported by the knowledge of their influ-ence on ecological functions. By contrast to other soil organisms,soil engineers are the only group impacting the four key aggre-gate ecosystem functions described by Kibblewhite et al. (2008).As decomposers, earthworms and termites consume litter and soilorganic matter (SOM), and then contribute to the release of min-eral nutrients in soil. As ecosystem engineers, they play a key role incontrolling the dynamics of soil structure in addition to the regula-tion of the abundance and activity of subordinate organisms, frommicroorganisms to plants (Jouquet et al., 2006). However, differentsoil engineers do not influence ecosystem functioning in the sameway and their influence on the four aggregated ecological func-tions depends on the interaction between their ecological strategyand their abiotic environment. Organisms are usually differentiatedinto functional groups according to their influence on specific eco-logical functions. These classifications can be based on both trophicand functional criteria, such as the classification of earthworms andtermites into extended or intended soil engineers (Jouquet et al.,2006), the distinction between epigeic, anecic and endogeic earth-worms (Bouché, 1977) or soil-feeding, litter-feeding and fungus-growing termites (Holt and Lepage, 2000; Jouquet et al., 2011a).These classifications can also be solely functional, such as in the caseof the compacting and decompacting earthworm species (Blanchartet al., 1997). Obviously, it is worth noticing that soil engineers canfavourably impact certain functions and others negatively. This isthe case of earthworms and termites that temporarily store SOMinto their casts and nests (function of C protection and service ofclimate regulation) but consequently reduce the release of mineralnutrients available to plants (function of nutrient cycling and ser-vice of food provisioning). It is therefore of primary importance toconsider all the functions impacted by soil engineers before decid-ing on the species to be used in soil restoration programmes (Fig. 2).

3. Methods to promote soil engineer activity

Direct and indirect methods exist to increase soil engineer activ-ity in the field. A direct method is simply to inoculate soil engineersin situ. This method only concerns the few earthworm speciesthat can easily be breed since it is difficult, slow or impossible tobreed termites, especially the soil-feeders and fungus-growing ter-mite species, under laboratory conditions (Jouquet et al., 2011a).Three main methods have been described and compared tooptimize earthworm breeding, inoculation and establishment ofhealthy populations in situ, namely the turf cutting and relaying,chemical/physical extraction with broadcasting and Earthworm

Inoculation Unit (EIU) methods. The advantages and disadvantagesof these methods have been discussed in several articles (Butt et al.,1995; Butt, 1999; Lowe and Butt, 2002, 2005; Butt, 2008; Eijsackers,2011). The main obstacle hampering direct earthworm inoculation

36 P. Jouquet et al. / Applied Soil

Targ et func�on(e.g. nu trient cycling)

Soil enginee rs

Restora�on

Side effec� unc�on(e.g. C protec�on)

Side-effect service(Climate re gula� on)

(Wat er qua lity)

Targ et service(Food provisioning)

Degrada�on

Ecosystem services

Fig. 2. Schematic representation of the influence of ecosystem engineers on ecolog-ical functions and ecosystem services. Programmes of restoration aim at stimulatingtarget functions (the nutrient cycling function in this example) but side-effect func-tions can also be stimulated or reduced (the C protection function in this example).As a consequence, the stimulation of soil engineer activity allows the restoration ofts

itam(frcsate

saadec2db2piogaraasa(g(

aoCo

species used to produce vermicompost are often exotic species

he target ecosystem service and increase of decrease side-effect ecosystem services,uch as climate regulation or water quality supply.

s the difficulty in obtaining enough earthworm individuals. Withhe exception of the few species available commercially as fish baitnd those used in vermitechnology that can be cultured artificially,ost of the species found in the field require artificial breeding

Lowe and Butt, 2005). Unfortunately, this process is not alwayseasible and can slow down rehabilitation programmes. For thiseason and because they tolerate a wider range of soil physico-hemical and climatic conditions than native species, exotic, andometimes invasive, species are sometimes preferred (e.g., Garcíand Fragoso, 2002; Ganihar, 2003). This leads to other environmen-al problems such as threats to local biodiversity and changes incosystem functions (González et al., 2006; Hale et al., 2006).

In the field, earthworms which are introduced into degradedoils often face inhospitable conditions (e.g. low soil moisturend nutritive resources and high pollutant concentrations) (Snydernd Hendrix, 2008). Consequently, improving environmental con-itions and selection of the appropriate earthworm species orcological category is of primary importance for ensuring their suc-essful establishment in the ecosystem (Butt, 2008; Mathieu et al.,010; Eijsackers, 2011). In some situations, re-vegetation of theegraded site or the application of lime and fertilizer are necessaryefore introducing earthworms (Robinson et al., 1992; Ganihar,003). In these situations, pre-treatments hasten the restorationrocesses. Surface litter and SOM influence soil structure and chem-

stry and act as source of food for earthworms and its quality is alsof major importance for the regulation of earthworm populationrowth. For example, depending on the organic resources avail-ble, endogeic species may be preferred to anecic species whichequire well established plants (for the provision of litter) or organicmendments (Butt, 1999; Langmaack et al., 2002). Conversely,necic earthworms may be preferred to endogeic earthworms inites with high levels of organic matter (Vimmerstedt, 1983). Incid soil, earthworms are absent for pH < 3.5 and sparse for pH < 4.5Muys and Granval, 1987; Curry, 2004) and acido-tolerant endo-eic species may be more suitable than less tolerant anecic speciesMuys and Granval, 1987; Rundgren, 1994; Muys et al., 2003).

The development of earthworm and termite populations canlso be fostered through indirect methods. Soil macrofauna devel-

pment is often limited by the quantity of available resources.onsequently, the application of mulch, organic amendments, lime,r the establishment of plant cover usually results in the expansion

Ecology 73 (2014) 34– 40

of local earthworm and termite species (Curry and Cotton, 1983;Rouland et al., 2003; Blanchart et al., 2006). However, a limitationof this approach relies in the fact that it does not allow a controlof the species (and the functions they can perform) that respondfavourably to the amendment of organic matter. The qualities ofthese organic resources are therefore of primary importance forthe selection of the targeted species (Curry and Boyle, 1987; Fraseret al., 2003). In agricultural systems, several studies also concludedthat no or low tillage are preferred management approaches tomore intensive farming practices, especially for the developmentof anecic species (Chan, 2004; Blanchart et al., 2006, 2007; Peignéet al., 2009). Although natural regeneration by termites is rapid(Rouland et al., 2003) because of their high dispersal rate (Arab andCosta-Leonardo, 2005; Nobre and Aanen, 2010; Nasir and Akhtar,2011) and allows development of termite populations in severalmonths to a few years (Mando et al., 1996; Mando and Brussaard,1999; Leonard and Rajot, 2001; Rouland et al., 2003; Léonard et al.,2004), this process is slower with earthworms in some systemsbecause their rate of spread is low in the field, from 1 to 10–13 m y−1

(Curry and Cotton, 1983; Ligthart and Peek, 1997; Nuutinen et al.,2006). Because these methods are indirect, their efficiency alsodepends on many uncontrolled parameters, such as the weatherand activity of other organisms which could slow down the devel-opment of the target soil engineers through competition and/orpredatory interactions. They also remain dependent on the capa-bility of soil macrofauna populations to colonize the sites from thesurrounding non-degraded ecosystems (Räty, 2004).

Another indirect method to use earthworm activity is theproduction of vermicompost (Edwards and Arancon, 2004). Thistechnology derived from ecological engineering relies on the exsitu intensification and externalization of ecological processes thattake place in the field. The interaction between epigeic earthwormsand microorganisms allows the degradation of organic residuesthrough mesophilic and aerobic processes and transforms theminto organic matter more stable than compost (Edwards et al.,2004). In the last two decades, vermitechnology has been appliedto the management of various types of wastes and sludge, toconvert them into vermicompost for increasing land fertility. Sur-prisingly, few studies have actually been made on the utilizationof this substrate produced by earthworms for soil restoration.However, recent studies carried out in Northern Vietnam tendto show that vermicompost could be useful for the rehabilitationof soils which have been degraded by soil erosion (Jouquet et al.,2011b; Ngo et al., 2011). Vermicompost applications can enhanceplant growth to the same extent as chemical fertilizers while soilproperties are greatly improved (higher soil pH, organic mattercontent, ammonium and cationic exchange capacity) and mineralnutrient losses considerably reduced (Jouquet et al., 2011b; Doanet al., 2013). However, although vermicompost is apparentlymore effective than compost at improving soil rehabilitation, thepositive influence of this substrate can be reduced in the presenceof the exotic earthworm species Dichogaster bolaui (Jouquet et al.,2010). In another study, Doan et al. (2013) also showed thatthe beneficial influence of compost and vermicompost on soilchemical properties can be reduced in presence of the endogeicspecies Metaphire posthuma. Although the reasons of this negativeinteraction between earthworms and vermicompost are unknown,two hypotheses were suggested: (i) a lower degradability of vermi-compost in comparison with compost and a possible competitionfor nutrients between microorganisms, plants and earthworms, (ii)a modification of soil physical parameters and a reduction of soilbulk density or hydraulic conductivity. Moreover, the earthworm

(i.e., the European species Eisenia fetida and E. andrei that arelargely used to produce vermicompost in all continents) and thesurvival, development and impact of these species in the field

d Soil

afvw

4

udtespatsHuSofplfrpiTv(

5

5

cmip1tpwtofi(tdwtlovrhne

5

t

P. Jouquet et al. / Applie

re unknown and require further investigations. Consequently,urther studies are needed on this topic to test the relevance of theermicomposting technology, and the interaction of vermicompostith local soil macrofauna for soil quality restoration in situ.

. Ecosystem restoration

In this section, we review the recent literature reporting thetilization of earthworms and termites for the rehabilitation ofegraded ecosystems. We have deliberately focused this review onhe rehabilitation of degraded ecosystems sensu stricto. Degradedcosystems are ecosystems which do not support or insufficientlyupport one or more targeted ecosystem services that they werereviously supporting (Bullock et al., 2011). This definition includesgroecosystems that were degraded by intensive industrialized cul-ivation practices with a reduction of their ability to ensure severalervices, such as those of production, water quality and erosion.owever, a large body of literature already exists on the potentialtilization of earthworm and termite activity for the restoration ofOM stocks, the control of nutrient cycling, and the improvementf plant growth and yield in agroecosystems. This review thereforeocuses on four less studied soil degradation types: acidic, com-acted or crusted, eroded and polluted soils. All are widespread

and degradation problems and result from the intensification ofarming practices, the unsustainable management of fertilizationegimes, waste disposal, the aerial deposition of acidifying com-ounds, mining and mine waste disposal (e.g., extraction of coal

n opencast mining or minerals possibly followed by land filling).hey have important consequences in the provision of the ser-ices of food provision (acidic and compacted soils), erosion controleroded soils) and detoxification (polluted soils).

. Service of food provisioning

.1. Acid soils

The common practice used to rehabilitate acid soils is the appli-ation of lime (CaCO3) to the soil surface. However, the downwardovement of lime to the rhizosphere, where it is the most needed,

s slow when tillage is not used. The process can be increased in theresence of anecic acido-tolerant earthworms (Muys and Granval,987; Curry, 2004). For instance, Chan (2003) showed in a labora-ory experiment that Aporrectodea longa could increase the subsoilH by 1.1 units (from 4.0 to 5.1) in the 7.5–10 cm layer after only 6eeks. The involved functions performed by earthworms are (i)

he downward diffusion of lime with water in vertical burrowspen to the surface (Baker et al., 1999), (ii) the ingestion of sur-ace lime by earthworms and its subsequent deposition in castsn the subsoil layer (Bengtsson and Rundgren, 1992; Chan, 2003),iii) the downward translocation of lime by physical attachment tohe body surface of earthworms (Chan, 2003), and (iv) and possiblyirect alkalinization due to cutaneous mucus excreted by earth-orms (Räty, 2004). Earthworms can also increase soil pH through

he consumption of litter and its incorporation in the soil humus-ayer (Räty, 2004; Ampoorter et al., 2011). However, the utilizationf earthworms to increase soil pH in acidic soils remains probablyery limited due to the absence of anecic earthworms in these envi-onments (Räty, 2004). Clearly, most of the studies on this topicave been done in laboratory experiments and more research isow needed in the field in order to assess the real potential ofarthworms to increase soil pH in acidic soils.

.2. Compacted and crusted soils

In temperate environments, earthworms have been suggestedo significantly contribute to the regeneration of compacted

Ecology 73 (2014) 34– 40 37

soils because of their burrowing and casting activity. However,this assessment results mainly from observations made underlaboratory conditions which overestimate soil regeneration byearthworms (Zund et al., 1997; Ponder et al., 2000; Larink et al.,2001; Langmaack et al., 2002). Indeed, field experiments showedthat soil compaction has a detrimental effect on earthworm abun-dance and activity (Söchtig and Larink, 1992; Radford et al., 2001)and that avoidance of compacted zones by earthworms is the gen-eral rule (Capowiez et al., 2009; Ampoorter et al., 2011). However,this negative effect of soil compaction on earthworms seems moreimportant with endogeic than anecic earthworms (Capowiez et al.,2009). As a consequence, it is likely that the potential of earthwormsto promote the rehabilitation of compacted soils remains limitedor is a slow process (Ampoorter et al., 2011; Capowiez et al., 2012).

In tropical countries, soil bulk density can be influenced by twoearthworm functional groups: the ‘compacting’ and ‘decompacting’species (Blanchart et al., 1997). Compacting earthworms producelarge size casts that decrease soil porosity where they are abundant,while decompacting species favour the fragmentation of large sizeaggregates and reduce soil bulk density. Although never tested, itis likely that the stimulation of the decompacting functional groupcould help restore soil structure in tropical environments (Barroset al., 2001). However, how to improve the activity of decompactingspecies in the detriment to compacting species remains an openquestion.

The ability of termites to develop in harsh environments andpromote water infiltration in crusted soils as part of soil reha-bilitation and vegetation cover regeneration has been strikinglydemonstrated in Africa (Mando et al., 1996; Mando and Brussaard,1999; Leonard and Rajot, 2001; Léonard et al., 2004), Asia (Pardeshiand Prusty, 2010) and Australia (Dawes, 2010). In these studies, theapplication of mulch or organic matter on or into the soil, as in thecase of the agricultural and forestry “zaï” systems (see Roose et al.,1999 for a description of the Zaï agricultural practice), triggeredtermite activity which then created burrows through the crustedsoil surface. This can result in an increase in water infiltration by afactor of 1.5–3 over a period of 3–4 years (Mando and Brussaard,1999; Leonard and Rajot, 2001), an increase in water retentionand a reduction in the bulk soil density of the upper soil layer.The change in soil characteristics due to termite activity is enoughto create the conditions necessary for natural vegetation develop-ment and then crop production on previously degraded bare soils.The main obstacle to the widespread uptake of these techniquesis that they are labour intensive. For instance the zaï techniquerequires 300 h ha−1 of work, as well as the availability and transportof 3000 kg ha−1 of organic substrates (Roose et al., 1999). Anotherinconvenience of this method is the difficulty in controlling organicamendment decomposition and the potential leaching of mineralnutrients (Fatondji et al., 2009).

6. Control of erosion

Earthworms and termites significantly influence water infil-tration, soil erosion and the transfer of nutrients throughoutecosystems. Although most of the literature concerns earthworms(see Blanchart et al., 2004 for a review), several studies also demon-strated a significant impact of termites (Jouquet et al., 2011a).Earthworms and termites reduce the risk of erosion throughthe production of burrows and subterranean nest structureswhich increase water infiltration, and through the production ofwater-stable aggregates (old earthworm casts and termite nests)

which enhance roughness, limiting surface runoff and protectthe soil from crusting (Blanchart et al., 2004; Evans et al., 2011;Jouquet et al., 2012). However, unstable biogenic aggregates (e.g.,freshly emitted earthworm casts, unstable granular or paste-like

3 d Soil

craJ

rwfrwgpboCw

7

oa2tetsitodAo(CNdctpwshmtawdttc

8

pttbeliamua

8 P. Jouquet et al. / Applie

asts, termite sheetings) accumulated on the soil surface fragmentapidly during rainfall events and increase soil and nutrient (Nnd P) exportation (Blanchart et al., 2004; Bottinelli et al., 2010;ouquet et al., 2012).

Surprisingly, the use of earthworm and termite activity toeduce the risk of soil erosion has never been tested. A first stepould probably be to identify species, or functional groups, which

avour water infiltration, reduce soil detachment and thus helpehabilitate ecosystems. This might be the case of anecic earth-orm species producing burrows open to the soil surface and

lobular water-stable casts, although these casts are also likely tolay a negative role by favouring soil loss when freshly emittedy earthworms (Le Bayon and Binet, 2001). This is also the casef fungus-growing termites producing open burrows for foraging.onversely, endogeic earthworms and soil feeder termite speciesould probably not be suitable for such a role.

. Detoxification

Numerous studies have examined the influence of earthwormsn heavy metal mobility in soil through their ingestion, burrowingnd casting activity (e.g., Vijver et al., 2003, 2007; Lukkari et al.,006; Qiu et al., 2011; Sizmur et al., 2011) or for the degrada-ion of soil pesticides and polycyclic aromatic hydrocarbons (Binett al., 2006; Schreck et al., 2008; Natal-da-Luz et al., 2012). Briefly,he introduction of earthworms usually facilitates the creation ofoil top layers, the establishment of vegetation (Baker et al., 2006),mproves primary production (Scullion and Malik, 2000), modifieshe mobility of metals, although this effect is variable, dependentn soil chemical properties and earthworm species and remainsifficult to predict. For instance, Lukkari et al. (2006) found thatporrectodea caliginosa decreases the mobility and bioavailabilityf Cu and Zn in soil through their burrowing activity. Sizmur et al.2011) showed that Lumbiscus terrestris decreased water solubleu and As but increased the solubility of Pb and Zn in soil, andatal-da-Luz et al. (2011) did not observed an influence of Den-robaena veneta on the solubility of Cr, Cu, Ni, and Zn in soil. As aonsequence, it is usually observed that earthworms increase phy-oextraction (Wang and Li, 2006; Jusselme et al., 2012). As outlinedreviously, significant improvement in the development of earth-orm populations is obtained following amendment with organic

ubstrates. For instance, the application of 10–25 Mg sewage sludgea−1 led to a two-fold increase in earthworm abundance in a postining soil in Germany (Emmerling and Paulsch, 2001). However,

he addition of organic substrates (compost) to contaminated soillso buffers metal solubility and thus reduces the effect of earth-orms on the solubility of metals (Sizmur et al., 2011). The mainisadvantage of using earthworms to restore open mined sites ishe possible accumulation of heavy metals or other pollutants inhe earthworms which could then become part of the trophic foodhain (Suthar and Singh, 2009).

. Towards more intensive soil restoration

Soil engineers have been described as ecosystem servicesroviders due to their importance in the maintenance of soil struc-ure and plant growth (Lavelle et al., 2006). However, althoughhere is a large body of literature stressing the key processesy which soil engineers influence ecosystem functioning, theirxploitation for the restoration of degraded ecosystems has beenargely unexplored (Fig. 1). In this review we have stressed themportance of soil engineers in restoration processes but we have

lso highlighted some of the obstacles hampering the develop-ent of this approach. Amongst these, all species are not always

seful for soil restoration programmes and preliminary studies arelways required to identify the most efficient species in terms of

Ecology 73 (2014) 34– 40

dispersion, colonization, demography and ecological functions.However, because soil engineers impact the four key aggregatedecological functions (Kibblewhite et al., 2008), their stimulationinfluence both targeted and side-effect functions with possiblepositive influence on the targeted ecosystem services but negativeinfluence on other ecosystem services. It is therefore importantto consider the whole set of functions impacted by soil engi-neers before their inoculation or indirect stimulation. Next, theutilization of soil macroinvertebrates to restore ecosystems is aslow process requiring several years to be effective (Ampoorteret al., 2011). It is also sometimes costly and labour-intensiveprocess. For instance, Butt (1999) estimated that the cost of theinoculation of earthworms in United Kingdom varied from 200to 6000 £ ha−1. At first glance, the inoculation approach appearsmore appropriate because of its faster outputs and our ability toselect species according to their roles on the four key aggregatedecological functions. However, from the 20 articles dealing withthe utilization of earthworms for restoring ecosystems, only fivestudies (Fraser et al., 2003; Muys et al., 2003; Blanchart et al.,2004; Ampoorter et al., 2011; Sizmur et al., 2011) were referencedsince the review of Butt (1999) and amongst them only three werecarried out in the field (Muys et al., 2003; Blanchart et al., 2004;Fraser et al., 2003). From these five trials, only three come to theconclusion about a potential positive influence of earthworms.Therefore, this shows both our need to extend trials in temperateand tropical ecosystems and to better chose species according totheir availabilities and impact on ecosystem functions. This reviewalso highlighted that most studies have focused on earthworms,mainly in temperate ecosystems, rather than termites (85 vs. 20,Fig. 1). One explanation lies in the fact that earthworms can bemore easily manipulated than termites, but another reason is thattermites suffer from a bad image, being seen mainly as pests ofcrops, trees and wood (Jouquet et al., 2011a).

Acknowledgments

As in any review, the concepts and ideas formulated in this arti-cle result from the dialogue with many colleagues and peers, whoare all acknowledged. We also thank the reviewers of this articlewho significantly helped in improving the manuscript.

References

Ampoorter, E., De Schrijver, A., De Frenne, P., Hermy, M., Verheyen, K., 2011. Exper-imental assessment of ecological restoration options for compacted forest soils.Ecological Engineering 37, 1734–1746.

Arab, A., Costa-Leonardo, A.M., 2005. Effect of biotic and abiotic factors on thetunneling behavior of Coptotermes gestroi and Heterotermes tenuis (Isoptera:Rhinotermitidae). Behavioural Processes 70, 32–40.

Baker, G.H., Carter, P.J., Barrett, V.J., 1999. Influence of earthworms, Aporrectodeaspp. (Lumbricidae), on lime burial in pasture soils in south-eastern Australia.Australian Journal of Soil Research 37, 831–845.

Baker, G.H., Brown, G., Butt, K., Curry, J.P., Scullion, J., 2006. Introduced earthworms inagricultural and reclaimed land: their ecology and influences on soil properties,plant production and other soil biota. Biological Invasions 8, 1301–1316.

Barrios, E., 2007. Soil biota, ecosystem services and land productivity. EcologicalEconomics 64, 269–285.

Barros, E., Curmi, P., Hallaire, V., Chauvel, A., Lavelle, P., 2001. The role of macrofaunain the transformation and reversibility of soil structure of an Oxisol in the processof forest to pasture conversion. Geoderma 100, 193–213.

Bengtsson, G., Rundgren, S., 1992. Seasonal variation of lead uptake in the earthwormLumbiscus terrestris and the influence of soil liming and acidification. Archivesof Environmental Contamination and Toxicology 23, 198–205.

Binet, F., Kersanté, A., Munier-Lamy, C., Le Bayon, R.C., Belgy, M.J., Shipitalo, M., 2006.Lumbricid macrofauna alter atrazine mineralization and sorption in a silt loamsoil. Soil Biology and Biochemistry 38, 1255–1263.

Blanchart, E., Lavelle, P., Braudeau, E., Le Bissonnais, Y., Valentin, C., 1997. Regulation

of soil structure by geophagous earthworm activities in humid savannas of Côted’Ivoire. Soil Biology and Biochemistry 29, 431–439.

Blanchart, E., Albrecht, A., Brown, G.G., Decaëns, T., Duboisset, A., Lavelle, P., Mariani,L., Roose, E., 2004. Effects of tropical endogeic earthworms on soil erosion: areview. Agriculture, Ecosystems and Environment 104, 303–315.

d Soil

B

B

B

B

B

B

B

B

B

B

C

C

C

C

C

C

C

C

D

D

D

d

D

E

E

E

E

E

F

F

P. Jouquet et al. / Applie

lanchart, E., Villenave, C., Viallatoux, A., Barthès, B., Girardin, C., Azontonde, A.,Feller, C., 2006. Long-term effect of a legume cover crop (Mucuna pruriens var.utilis) on the communities of soil macrofauna and nematofauna, under maizecultivation, in southern Benin. European Journal of Soil Biology 42, 136–144.

lanchart, E., Bernoux, M., Sarda, X., Siqueira Neto, M., Cerri, C.C., Piccolo, M., Douzet,K.M., Scopel, E., Feller, C., 2007. Effect of direct seeding mulch-based systems onsoil carbon storage and macrofauna in Central Brazil. Agriculturae ConspectusScientificus 72, 81–87.

louin, M., Hodson, M.E., Delgado, E.A., Baker, G., Brussaard, L., Butt, K.R., Dai, J.,Dendooven, L., Peres, G., Tondoh, J.E., Cluzeau, D., Brun, J.J., 2013. A review ofearthworm impact on soil function and ecosystem services. European Journal ofSoil Science 6, 161–162.

ottinelli, N., Henry-des-Tureaux, T., Hallaire, V., Mathieu, J., Benard, Y., Tran, T.D.,Jouquet, P., 2010. Earthworms accelerate soil porosity turnover under wateringconditions. Geoderma 156, 43–47.

ouché, M.B., 1977. Stratégies lombriciennes. In: Lohn, U., Persson, T. (Eds.), SoilOrganisms as Components of Ecosystems, 25. Ecology Bulletin, Stockholm,pp. 122–132.

rown, J., Scholtz, C.H., Janeau, J.L., Grellier, S., Podwojewski, P., 2010. Dung beetles(Coleoptera: Scarabaeidae) can improve soil hydrological properties. AppliedSoil Ecology 46, 9–16.

ullock, J.M., Aronson, J., Newton, A.C., Pywell, R.F., Rey-Benayas, J.M., 2011. Restora-tion of ecosystem services and biodiversity: conflicts and opportunities. TREE26, 541–549.

utt, K.R., Frederickson, J., Morris, R.M., 1995. An earthworm cultivation and soilinoculation technique for land restoration. Ecological Engineering 4, 1–9.

utt, K.R., 1999. Inoculation of earthworms into reclaimed soils: the UK experience.Land Degradation and Development 10, 565–575.

utt, K.R., 2008. Earthworms in soil restoration: lessons learned from United King-dom case studies of land reclamation. Restoration Ecology 16, 637–641.

apowiez, Y., Cadoux, S., Bouchand, P., Roger-Estrade, J., Richard, G., Boizard, H.,2009. Experimental evidence for the role of earthworms in compacted soilregeneration based on field observations and results from a semi-field experi-ment. Soil Biology and Biochemistry 41, 711–717.

apowiez, Y., Sammartino, S., Cadoux, S., Bouchant, P., Richard, G., Boizard, H., 2012.Role of earthworms in regenerating soil structure after compaction in reducedtillage systems. Soil Biology and Biochemistry 55, 93–103.

han, K.Y., 2003. Using earthworms to incorporate lime into subsoil to ameliorateacidity. Communications in Soil Science and Plant Analysis 34, 985–997.

han, K.Y., 2004. Impact of tillage practices and burrows of a native Australian anecicearthworm on soil hydrology. Applied Soil Ecology 27, 89–96.

ostanza, R., Arge, R., deGroot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K.,Naeem, S., Oneill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., vandenBelt, M., 1997.The value of the world’s ecosystem services and natural capital. Nature 387,253–260.

urry, J.P., Cotton, D.C.F., 1983. Earthworms and land reclamation. In: Satchell, J.E.(Ed.), Earthworm Ecology, from Darwin to Vermiculture, 18. Chapman and Hall,London, New York, pp. 215–228.

urry, J.P., Boyle, K.E., 1987. Growth rates, establishment, and effects on herbageyield of introduced earthworms in grassland on reclaimed cutover peat. Biologyand Fertility of Soils 3, 95–98.

urry, J.P., 2004. Factors affecting the abundance of earthworms in soils. In:Edwards, C.A. (Ed.), Earthworm Ecology. CRC Press, Boca Raton, FL, USA, pp. 91–113.

awes, T.Z., 2010. Reestablishment of ecological functioning by mulching and ter-mite invasion in a degraded soil in an Australian savanna. Soil Biology andBiochemistry 42, 1825–1834.

oan, T.T., Ngo, T.P., Rumpel, C., Nguyen, V.B., Jouquet, P., 2013. Interactions betweencompost, vermicompost and earthworm influence plant growth and yield. A oneyear greenhouse experiment. Scientia Horticulturae 160, 148–154.

e Goede, R.M.G., Brussaard, L., 2002. Soil zoology: an indispensable component ofintegrated ecosystem studies. European Journal of Soil Biology 38, 1–6.

e Groot, R.S., Wilson, M.A., Boumans, R.M.J., 2002. A typology for the classification,description and valuation of ecosystem functions, goods and services. EcologicalEconomics 41, 393–408.

unger, W., Voigtländer, K., 2005. Assessment of biological soil quality in woodedreclaimed mine sites. Geoderma 129, 32–44.

dwards, C.E., Arancon, N., 2004. The use of earthworms in the breakdown of organicwastes to produce. In: Edwards, C.A. (Ed.), Earthworm Ecology. CRC Press, BocaRaton, FL, USA, pp. 345–371.

dwards, C.E., Dominguez, J., Norman, Q.A., 2004. The influence of vermicompostson plant growth and pest incidence. Soil Zoology for Sustainable Developmentin the 21st century. S.H. Shakir, Mikhail, W.Z.A., self-publisher, Le Caire. 18,397–420.

ijsackers, H., 2011. Earthworms as colonizers of natural and cultivated soil envi-ronments. Applied Soil Ecology 50, 1–13.

mmerling, C., Paulsch, D., 2001. Improvement of earthworm (Lumbricidae) com-munity and activity in mine soils from open-cast coal mining by the applicationof different organic waste materials. Pedobiology 45, 396–407.

vans, T.A., Dawes, T.Z., Ward, P.R., Lo, N.T., 2011. Ants and termites increase cropyield in a dry climate. Nature Communication 2, 262.

atondji, D., Martius, C., Bielders, C.L., Koala, S., Vlek, P.L.G., Zougmore, R., 2009.Decomposition of organic amendment and nutrient release under the zai tech-nique in the Sahel. Nutrient Cycling in Agroecosystems 85, 225–239.

raser, P.M., Beare, M.H., Butler, R.C., Harrison-Kirk, T., Piercy, J.E., 2003. Interactionsbetween earthworms (Aporrectodea caliginosa), plants and crop residues for

Ecology 73 (2014) 34– 40 39

restoring properties of a degraded arable soilL: the 7th international symposiumon earthworm ecology Cardiff Wales 2002. Pedobiology 47, 870–876.

Ganihar, S.R., 2003. Nutrient mineralization and leaf litter preference by the earth-worm Pontoscolex corethrurus on iron ore mine wastes. Restoration Ecology 11,475–482.

García, J.A., Fragoso, C., 2002. Influence of different food substrates on growth andreproduction of two tropical earthworm species (Pontoscolex corethrurus andAmynthas corticis). Pedobiology 47, 754–763.

González, G., Huang, C.Y., Zou, X., Rodríguez, C., 2006. Earthworm invasions in thetropics. Biological Invasions 8, 1247–1256.

Hale, C.M., Frelich, L.E., Reich, P.B., 2006. Changes in hardwood forest understoryplant communities in response to European earthworm invasions. Ecology 87,1637–1649.

Holt, A.J., Lepage, M., 2000. Termites and soil properties. In: Abe, B.T.D.E., Higashi, M.(Eds.), Termites: Evolution, Sociality, Symbioses, Ecology, 18. Kluwer AcademicPublishers, Netherlands, pp. 389–407.

Jones, D.T., Susilo, F.X., Bignell, D.E., Hardiwinoto, S., Gillison, A.N., Eggleton, P., 2003.Termite assemblage collapse along a land-use intensification gradient in low-land central Sumatra, Indonesia. Journal of Applied Ecology 40, 380–391.

Jouquet, P., Dauber, J., Lagerlof, J., Lavelle, P., Lepage, M., 2006. Soil invertebratesas ecosystem engineers: intended and accidental effects on soil and feedbackloops. Applied Soil Ecology 32, 153–164.

Jouquet, P., Plumere, T., Doan Thu, T., Rumpel, C., Tran Duc, T., Orange, D.,2010. The rehabilitation of tropical soils using compost and vermicompost isaffected by the presence of endogeic earthworms. Applied Soil Ecology 46,125–133.

Jouquet, P., Traoré, S., Choosai, C., Hartmann, C., Bignell, D., 2011a. Influence oftermites on ecosystem functioning: ecosystem services provided by termites.European Journal of Soil Biology 47, 215–222.

Jouquet, P., Bloquel, E., Thu Doan, T., Ricoy, M., Orange, D., Rumpel, C., Tran Duc, T.,2011b. Does compost and vermicompost improve macronutrient retention andplant growth in degraded tropical soils? Compost Science and Utilization 19,15–24.

Jouquet, P., Janeau, J.L., Pisano, A., Tran Sy, H., Orange, D., Luu Thi Nguyet, M., Valentin,C., 2012. Influence of earthworms and termites on runoff and erosion in a tropicalsteep slope fallow in Vietnam: a rainfall simulation experiment. Applied SoilEcology 61, 161–168.

Jusselme, M.D., Poly, F., Miambi, E., Mora, P., Blouin, M., Pando, A., Rouland-Lefèvre,C., 2012. Effect of earthworms on plant Lantana camara Pb-uptake and on bac-terial communities in root-adhering soil. Science of the Total Environment 416,200–207.

Kibblewhite, M.G., Ritz, K., Swift, M.J., 2008. Soil health in agricultural systems. Philo-sophical Transactions of the Royal Society B–Biolgical Science 363, 685–701.

Langmaack, M., Schrader, S., Rapp-Bernhardt, U., Kotzke, K., 2002. Soil structurerehabilitation of arable soil degraded by compaction. Geoderma 105, 141–152.

Larink, O., Werner, D., Langmaack, M., Schrader, S., 2001. Regeneration of compactedsoil aggregates by earthworm activity. Biology and Fertility of Soils 33, 395–401.

Lavelle, P., Bignell, D., Lepage, M., 1997. Soil function in a changing world: the role ofinvertebrate ecosystem engineers. European Journal of Soil Biology 33, 159–193.

Lavelle, P., Spain, A.V., 2001. Soil Ecology. Kluwer Academic, Dordrecht, TheNeherlands, 654 pp.

Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Blouin, M., Bureau, F., Margerie, P., Mora,P., Rossi, J.P., 2006. Soil invertebrates and ecosystem services. European Journalof Soil Biology 42, 3–15.

Le Bayon, R.C., Binet, F., 2001. Earthworm surface casts affect soil erosion by runoffwater and phosphorus transfer in a temperate maize crop. Pedobiology 45,430–442.

Leonard, J., Rajot, J.L., 2001. Influence of termites on runoff and infiltration: quan-tification and analysis. Geoderma 104, 17–40.

Léonard, J., Perrier, E., Rajot, J.L., 2004. Biological macropores effect on runoff andinfiltration: a combined experimental and modelling approach. Agriculture,Ecosystems and Environment 104, 277–285.

Ligthart, T.N., Peek, G., 1997. Evolution of earthworm burrow systems after inocula-tion of lumbricid earthworms in a pasture in the Netherlands. Soil Biology andBiochemistry 29, 453–462.

Lowe, C.N., Butt, K.R., 2002. Influence of organic matter on earthworm productionand behaviour: a laboratory-based approach with applications for soil restora-tion. European Journal of Soil Biology 38, 173–176.

Lowe, C.N., Butt, K.R., 2005. Culture techniques for soil dwelling earthworms: areview. Pedobiology 49, 401–403.

Lukkari, T., Teno, S., Väisänen, A., Haimi, J., 2006. Effects of earthworms on decom-position and metal availability in contaminated soil: microcosm studies ofpopulations with different exposure histories. Soil Biology and Biochemistry38, 359–370.

Majer, J.D., Brennan, K.E.C., Moir, M.L., 2007. Invertebrates and the restoration ofa forest ecosystem: 30 years of research following bauxite mining in westernAustralia. Restoration Ecology 15, 104–115.

Mathieu, J., Barot, S., Blouin, M., Caro, G., Decaëns, T., Dubs, F., Dupont, L., Jouquet,P., Nai, P., 2010. Habitat quality, conspecific density, and habitat pre-use affectthe dispersal behaviour of two earthworm species, aporrectodea icterica anddendrobaena venata, in a mesocosm experiment. Soil Biology and Biochemistry

42, 203–209.

Mando, A., Stroosnijder, L., Brussaard, L., 1996. Effects of termites on infiltration intocrusted soil. Geoderma 74, 107–113.

Mando, A., Brussaard, L., 1999. Contribution of termites to the breakdown of strawunder Sahelian conditions. Biology and Fertility of Soils 29, 332–334.

4 d Soil

M

M

N

N

N

N

N

N

P

P

P

P

Q

R

R

R

R

0 P. Jouquet et al. / Applie

uys, B., Granval, P., 1987. Earthworms as bio-indicators of forest site quality. SoilBiology and Biochemistry 29, 323–328.

uys, B., Beckers, G., Nachtergale, L., Lust, N., Merckx, R., Granval, P., 2003. Mediumterm evaluation of a forest soil restoration trial combining tree species change,fertilisation and earthworm introduction. Pedobiology 47, 772–783.

atal-da-Luz, T., Ojeda, G., Costa, M., Pratas, J., Lanno, R.P., Van Gestel, C.A.M., Sousa,J.P., 2011. Short-term changes of metal availability in soil. II: the influence ofearthworm activity. Applied Soil Ecology 49, 178–186.

atal-da-Luz, T., Lee, I., Verweij, R.A., Morais, P.V., Van Velzen, M.J.M., Sousa, J.P., VanGestel, C.A.M., 2012. Influence of earthworm activity on microbial communitiesrelated with the degradation of persistent pollutants. Environmental Toxicologyand Chemistry 31, 794–803.

asir, S., Akhtar, M.S., 2011. Swarming of termites (Isoptera) in the Mianwali District.Pakistan Sociobiology 58, 151–164.

obre, T., Aanen, D.K., 2010. Dispersion and colonisation by fungus-growing ter-mites: vertical transmission of the symbiont helps, but then. . .? Communicativeand Integrative Biology 3, 248–250.

go, P.T., Rumpel, C., Dignac, M.F., Billou, D., Tran, D.T., Jouquet, P., 2011. Transfor-mation of Buffalo manure by composting or vermicomposting to rehabilitatedegraded tropical soils. Ecological Engineering 37, 269–276.

uutinen, V., Nieminen, M., Butt, K.R., 2006. Introducing deep burrowing earth-worms (Lumbricus terrestris L.) into arable heavy clay under boreal conditions.European Journal of Soil Biology 42, 269–274.

aoletti, M., 1999. The role of earthworms for assessment of sustainability and asbioindicators. Agriculture, Ecosystems and Environment 74, 137–155.

ardeshi, M., Prusty, B.A.K., 2010. Termites as ecosystem engineers and potentialsfor soil restoration. Current Science India 99, 11.

eigné, J., Cannavaciuolo, M., Gautronneau, Y., Aveline, A., Giteau, J.L., Cluzeau, D.,2009. Earthworm populations under different tillage systems in organic farming.Soil and Tillage Research 104, 207–214.

onder, F., Li, F.M., Jordan, D., Berry, E.C., 2000. Assessing the impact of Diplocardiaornata on physical and chemical properties of compacted forest soil in micro-cosms. Biology and Fertility of Soils 32, 166–172.

iu, H., Vijver, M.G., Peijnenburg, W., 2011. Interactions of cadmium and zinc impacttheir texocity to the earthworm Aporrectodea caliginosa. Environmental Toxico-logy and Chemistry 30, 2084–2093.

abary, B., Blanchart, E., Andriamanantena, Z., Hervouet, C., Douzet, J.M., Michel-lon, R., Moussa, N., Chotte, J.L., 2008. Activités biologiques et dynamique de lamatière organique du sol sous systèmes de culture en semis direct sur couver-ture végétale (Hauts plateaux de Madagascar). Terre malgache 26, 29–33.

adford, B.J., Wilson-Rummenie, A.C., Simpson, G.B., Bell, K.L., Ferguson, M.A., 2001.Compacted soil affects soil macrofauna populations in a semi-arid environmentin central Queensland. Soil Biology and Biochemistry 33, 1869–1872.

äty, M., 2004. Growth of Lumbricus terrestris and Aporrectodea caliginosa in an acid

forest soil, and their effects on enchytraeid populations and soil properties.Pedobiology 48, 321–328.

obinson, C.H., Piearce, T.G., Ineson, P., Dickson, D.A., Nys, C., 1992. Earthworm com-munities of limed coniferous soils: field observations and implications for forestmanagement. Forest Ecology and Management 55, 117–134.

Ecology 73 (2014) 34– 40

Roose, E., Kaboré, V., Guenat, C., 1999. Zaï practice: a West African traditional reha-bilitation system for semiarid degraded lands, a case study in Burkina Faso. AridSoil Research and Rehabilitation 13, 343–355.

Rouland, C., Lepage, M., Chotte, J.L., Diouf, M., Ndiaye, D., Ndiaye, S., Seuge, C.,Brauman, A., 2003. Experimental manipulation of termites (Isoptera, Macroter-mitinae) foraging patterns in a Sahelo-Sudanese savanna: effect of litter quality.Insectes Sociaux 50, 309–316.

Ruiz, N., Mathieu, J., Célini, L., Rollard, C., Hommay, G., Iorio, E., Lavelle, P., 2011. IBQS:a synthetic index of soil quality based on soil macro-invertebrate communities.Soil Biology and Biochemistry 43, 2032–2045.

Rundgren, S., 1994. Earthworms and soil remediation. Liming of acidic coniferousforest soils and Southern Sweden. Pedobiology 38, 519–529.

Schreck, E., Geret, F., Gontier, L., Treilhou, M., 2008. Neurotoxic effect and metabolicresponses induced by a mixture of six pesticides on the earthworm Aporrectodeacaliginosa nocturna. Chemosphere 71, 1832–1839.

Scullion, J., Malik, A., 2000. Earthworm activity affecting organic matter, aggrega-tion and microbial activity in soils restored after opencast mining for coal. SoilBiology and Biochemistry 32, 119–126.

Sizmur, T., Palumbo-Roe, B., Hodson, M.E., 2011. Impact of earthworms on trace ele-ment solubility in contaminated mine soils amended with green waste compost.Environmental Pollution 159, 1852–1860.

Snyder, B.A., Hendrix, P., 2008. Current and potential roles of soil macroinvertebrates(Earthworms, Millipedes, and Isopods) in ecological restoration. RestorationEcology 16, 629–636.

Söchtig, W., Larink, O., 1992. Effect of soil compaction on activity and biomassof endogeic lumbricids in arable soils. Soil Biology and Biochemistry 24,1595–1599.

Suthar, S., Singh, S., 2009. Bioconcentrations of metals (Fe, Cu, Zn, Pb) in earthworms(Eisenia foetida), inoculated in municipal sewage sludge: do earthworms pose apossible risk of terrestrial food chain contamination? Environmental Toxicology24, 25–32.

Toyota, A., Kaneko, N., Ito, M.T., 2006. Soil ecosystem engineering by the trainmillipede Parafontaria laminata in a Japanese larch forest. Soil Biology and Bio-chemistry 38, 1840–1850.

Vijver, M.G., Vink, J.P.M., Miermans, C.J.H., van Gestel, C.A.M., 2003. Oral sealingusing glue: a new method to distinguish between intestinal and dermal uptakeof metals in earthworms. Soil Biology and Biochemistry 35, 125–132.

Vijver, M.G., Vink, J.P.M., Miermans, C.J.H., van Gestel, C.A.M., 2007. Metal accumu-lation in earthworms inhabiting floodplain soils. Environmental Pollution 148,132–140.

Vimmerstedt, J.P., 1983. Earthworm ecology in reclaimed opencast coal mining sitesin Ohio. In: Satchell, J.E. (Ed.), Earthworm Ecology. From Darwin to Vermiculture,19. Chapman and Hall, London, New York, pp. 229–240.

Wang, D., Li, H., 2006. Effect of earthworms on the phytoremediation of zinc-

polluted soil by ryegrass and Indian mustard. Biology and Fertility of Soils 43,120–123.

Zund, P.R., Pillai-McGarry, U., McGarry, D., Bray, S.G., 1997. Repair of a com-pacted Oxisol by the earthworm Pontoscolex corethrurus (Glossoscolecidae,Oligochaeta). Biology and Fertility of Soils 25, 202–208.