Impacts of earthworms on soil components and dynamics… · Impacts of earthworms on soil components and dynamics 123 density, as did microbial metabolic activity. In addition, Coq

BASE Biotechnol. Agron. Soc. Environ.201418(1),121-133 Focus on:

Impactsofearthwormsonsoilcomponentsanddynamics.AreviewAboulkacemLemtiri(1),GillesColinet(2),TaoficAlabi(1),DanielCluzeau(3),LaraZirbes(1),ÉricHaubruge(1),FrédéricFrancis(1)(1)Univ.Liege-GemblouxAgro-BioTech.FunctionalandEvolutionaryEntomology.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:[email protected](2)Univ.Liege-GemblouxAgro-BioTech.DepartmentofEnvironmentalSciencesandTechnologies.Soil–WaterSystems.PassagedesDéportés,2.B-5030Gembloux(Belgium).(3)UniversitéEuropéennedeBretagne.UMRCNRS/URennes1EcoBio.StationBiologique.35380Paimpont(France).

ReceivedonOctober9,2012;acceptedonAugust20,2013.

Earthwormpopulationsareimportantdecomposerscontributingtoaggregateformationandnutrientcyclingprocessesinvolvingnitrogencycles,phosphorusandcarbon.Theyareknowntoinfluencesoilfertilitybyparticipatingtoimportantprocessesinsoilsuchassoilstructureregulationandorganicmatterdynamics.Earthwormsalsomodifythemicrobialcommunitiesthroughdigestion,stimulationanddispersionincasts.Consequently,changesintheactivitiesofearthwormcommunities,asaresultofsoilmanagementpractices,canalsobeusedasindicatorsofsoilfertilityandquality.Itisthereforeimportanttounderstandhowearthwormcommunitiesaffectsoildynamics.Thisreviewadressesthecurrentstateofknowledgeonearthworm’simpactsonsoilstructureandsoilorganicmatter(carbon,nitrogen,andphosphorus)dynamics,withspecialemphasisontheeffectsoflandmanagementpracticesonearthwormcommunities.Keywords.Earthworms,Oligochaeta,nutrientcyclinginecosystems,microbialcommunities,soilorganicmatterdynamics,soilfertility,agriculturalpractices.

Impacts des vers de terre sur les composants et la dynamique du sol (synthèse bibliographique). Lesversdeterresontdesdécomposeursimportantscontribuantàlaformationd’aggrégatsetauxdifférentscyclesd’élémentsnutritifstelsquel’azote,lephosphoreetlecarbone.Ilssontconnuspourleurinfluencesurlafertilitédusolenparticipantàlarégulationdelastructuredusoletàladynamiquedelamatièreorganique.Eningérantd’importantesquantitésdesol,lesversdeterremodifientlacommunautémicrobiennelorsdupassageàtraversleurtubedigestif.Parconséquent,leschangementsdanslesactivitésdelacommunautélombricienne,àlasuitedepratiquesdegestiondessols,peuventégalementêtreutiliséscommeindicateursdelafertilitéetdelaqualitédessols.Ilestimportantdecomprendrecommentlescommunautéslombriciennesaffectentladynamiquedessols.Cettesynthèsebibliographiqueportesurl’étatactueldesconnaissancessurlesimpactsdeversdeterresurlastructuredessolsetladynamiquedelamatièreorganique,enmettantl’accentsurlesimpactsdespratiquesagricolessurlescommunautéslombriciennes.Mots-clés.Verdeterre,Oligochaeta,cyclesnutrimentsdansécosystèmes,floremicrobienne,matièreorganiquedusol,fertilitédusol,pratiqueagricole.

1. INTRODUCTION

Soil formsanarrowinterfacebetweentheatmosphereandthelithosphere.Thestructureofcultivatedsoilresultsfromclimatic,anthropogenic,andbiologicalprocesses,butthepreciserolesofeachoftheseprocessesisdifficultto assess. The impact of earthworms activity on soilstructurewasunderlinedlongago,andtheseorganismsare now recognized as major biological drivers intemperateagrosystems.Soilcharacteristics(pH,organicmatter, nitrogen, granulometry, etc.) are influencedby

earthwormsbecausetheyparticipateintheconstructionand destruction of the soil particles, as well as inorganicmattertransfer.Thesoilingestedbyearthwormsundergoes chemical and microbial changes when itpassesthroughtthegut.OrganicmatterisdigestedandboththepHandthemicrobialactivityofthegutcontentsincrease (Edwards et al., 1996; Lukkari et al., 2006).Earthworms accelerate nitrogen mineralization fromorganicmatter,buttheeffectdependsonthespeciesandtheirinteractionwithsoilcharacteristics,organicmatterlocationandsoilbiota(Butenschoenetal.,2009).

122 Biotechnol. Agron. Soc. Environ. 201418(1),121-133 LemtiriA.,ColinetG.,AlabiT.etal.

Soil biodiversity has been widely studied sincethesoilitselfisthebaseforfarming(Stockdaleetal.,2006).Theconservationofbiodiversityisnecessarytomaintain thesustainablefunctioningofsoil. In1881,Darwinwasoneof thefirstscientistswhonotedthatthe topsoil consisted mostly of earthworm castings,thus highlighting the importance of earthwormsin pedogenesis processes (soil organo-mineralcomplex). For example, the earthworm populationbuildsgalleriesandingestslargequantitiesoforganicandmineralmatter, thusmodifying the porosity andaggregation of the soil.This earthworm bioturbationmaysubsequentlybereflectedinsoilprofiles(Zhanget al., 1995), for example: soil profile disturbance,soilstructuremodification,andverticalandhorizontalredistribution of soil and organicmatter (OM). Thisredistribution of OM depends on the earthwormecologicalgroups.Endogeicearthwormskeepmovinginside the soil to feed on soil organicmatter (SOM)while anecic ones feed on plant litter and organicresidues at the soil surface and tend to stay in thesame burrow (Lavelle et al., 1997). Epigeic species,which consume considerable amounts of raw OMhaveabroadrangeofenzymaticcapacities,probablymainly originating from ingested microflora (Curryetal.,2007).AsdiscussedbyLavelle(1997),thesoilbiogenic structure (mixture of casts, burrows, OM,etc.)createdbyearthworms iscommonly termed the“drilosphere”(Brownetal.,2000).

In agrosystems, the intensification of humanactivities (tillage, use ofmineral fertilizers, etc.) hasled to deterioration in structural and biological soilcharacteristics (Edwards, 1984; Lee, 1985). Soildegradation is often associated with decreases inbiodiversity and the abundances of earthworms andother invertebrate communities (Lee et al., 1991;Lavelle,1997).However,thereisaperceivedlackofinformationtocharacterizeadequatelytheirfunctionalrole in soil ecosystem processes such as soil carbonsequestration and loss, decomposition of organicresidues,andthemaintenanceofsoilstructure.

Thispaperaddressesthecurrentstateofknowledgeon earthworms’ impacts on soil structure and SOM(carbon, nitrogen, and phosphorus) dynamics, withspecial emphasis on the effects of landmanagementpracticesonearthwormcommunities.

2. THE ROLE OF EARTHWORMS IN ORGANIC MATTER DECOMPOSITION AND NUTRIENT DYNAMICS

2.1. Decomposition of organic matter

Organicmatter(OM)ismainlypresentinthetop20–30cmofmostsoilprofilesandisessentiallyanarray

of organic macromolecules consisting principally ofcombinationsofcarbon(C),oxygen(O)hydrogen(H),nitrogen (N), phosphorus (P) and sulfur (S).Almostall OM in soil is directly or indirectly derived fromplants via photosynthesis. Specifically, atmosphericcarbondioxideistransformedbyreductionintosimpleandcomplexorganiccarbon(OC)compounds,whichincombinationwithkeynutrientsenabletheplant tofunctionandgrow.Soilorganicmatter(SOM)providesfood and substrates for soil organisms, ranging frommacroinvertebrates to heterotrophic bacteria (Lavelleetal.,2001).Thisisofgreatimportance,giventhatthesoilbiotaisincreasinglyrecognizedasplayingamajorrole in soil functions. In cultivated soils, earthwormcommunities could play an important role in SOMdynamicsthroughregulationofthemineralizationandhumificationprocesses (Lavelle et al., 1992).On thebasisoftheresultsofcurrentliterature,itappearsthattherearesomedifferencesamongstudiesregardingtheeffectsofearthwormsonsoilorganiccarboncontent.Lachnichtetal.(1997)andDesjardinsetal.(2003)foundanegativeeffectofearthwormsadditiononsoilcarboncontent,whereasGilot(1997)foundanoppositeeffect.IntheexperimentofDesjardinsetal.(2003),themaizecropwasgrownunderno tillage, and this factor canexplaintheweaklossofcarboninthenon-inoculatedplots.Thedecreaseby28%ofthetotalcarboncontentin the earthworm-inoculated plots indicates that theendogeictropicalearthwormPontoscolex corethrurusaffectstheSOMdynamicsdramatically.TheobservedlossesofSOMincontinuouslycroppedfieldsareoftenattributedtoarapidmineralizationofSOMfollowingcultivation. Earthworms caused a decrease in SOMand carbonmineralization bymobilizing recalcitrantforms of OM. Earthworms enhance mineralizationby fragmenting SOM and by mixing SOM, mineralparticles and microorganisms, thus creating newcontactsurfacesbetweentheSOMandmicroorganisms(Parmeleeetal.,1998).Sinceearthwormsofdifferentecological groups prefer different food resources,they likely affect nutrient mineralization. Anecicearthwormsincorporatelittermaterialintothemineralsoiltherebymakingitavailableforthesoilfoodweb(Bossuyt et al., 2006). Endogeic earthworm species,in contrasts, primarily consume soil and associatedhumifiedOMintheupperlayerofthemineralsoil.

Soil microorganisms, mainly fungi and bacteria,are primarily responsible for the transformation oforganic molecules in soil, and their activity is thusa key factor in SOM dynamics (Coq et al., 2007).Aira et al. (2008) characterized changes in fungalpopulations, bacterivore nematodes communities andthe biochemical properties of an organic substrateover a short (72h) exposure to four densities of theepigeic earthworm Eisenia fetida. Calcium andN-mineralizationincreasedwithincreasingearthworms

Impactsofearthwormsonsoilcomponentsanddynamics 123

density,asdidmicrobialmetabolicactivity.Inaddition,Coqetal.(2007)showedthatcastsofendogeicspeciesPontoscolex corethrurus were slightly enriched in Cand showed significantly higher mineralization thanthe non-ingested soil. The higher mineralization incastsmight indicate a higher concentration of labilecompounds(solublecarbon,lignin,etc.),andprobablyahighermicrobialactivity.Earthwormshaveindirecteffects on soil organic carbon as determinants ofmicrobial activity. In addition, mucus productionassociatedwithwater excretion in the earthwomgutis known to enhance the microbial activity (Barois,1986).

Insoil,earthwormscontrolbiomass,diversityandactivityof soilmicroorganisms (Doubeet al., 1998).However,microorganismsmayconstituteanimportantpartofthedietofearthworms,whichcanfeedonthemselectively (Moody et al., 1995; Edwards, 2004). Inmostnaturalandmanagedecosystems,uptohalfoftheOCaddedtosoilonanannualbasisbyplantdetritusandrootexudatesisrapidlyconsumedbymicroorganisms,andreleasedascarbondioxide(Hopkinsetal.,2005;Wolf et al., 2005).The remainder of the addedOM,together with organic compounds synthesized bysoil organisms during decomposition and which isreleasedmainly as detritus, persist in the soil for anextended period. The importance of soil fauna inthe decomposition of OM is well known. However,the complex interactions between earthworm andsoil microorganisms are less understood.While soilinvertebratesyieldabout15%oftheCand30%oftheNinsomeecosystems(Anderson,1995),theirindirecteffectsthroughactivationofmicrofloraarelikelytobemuchgreater.

2.2. Consumption and humification

Epigeic earthworm species may feed directly onmicroorganisms or litter material and inhabit theorganic layer of soil. They have been shown tostrongly affect decomposition processes (Sampedroet al., 2008) and modify the fungal composition offorestsoils(McLeanetal.,2000).Generally,effectsofearthwormsonmicrobialbiomassandactivitydependon soil conditions (Shaw et al., 1986;Wolters et al.,1992).

Aira et al. (2006) showed thatmicrobial biomassandactivityinpigslurryweresignificantlydecreasedby transit through the gut of the epigeic speciesEudrilus eugeniae.ItappearsthatE. eugeniaeisabletodigestmicroorganismspresentinpigslurry(Airaetal.,2006).Theeffectsofearthwormsonmicroorganismsdepend on the kind of food source and availabilityandthespeciesofearthwormsinvolved(Flegeletal.,2000;Tiunovetal.,2000).McLeanetal.(2006)foundthatinvasiveearthwormsdecreasedmicrobialbiomass

insurfacesoilswithahighorganiccarboncontentandincreasedmicrobialbiomassintheunderlyingmineralsoils.Zhangetal.(2000)foundthatlargenumbersofthe anecic earthwormMetaphire guillelmi decreasedmicrobial biomass C, N and P after 24h, therebyconcludingthatearthwormsusedmicroorganismsasasecondaryfoodsource.

An attempt to distinguish between nutrient-enrichment processes associated with the OMincorporationandgut-associatedprocessesassociatedwith the passage of soil andOM through the gut ofLumbricus terrestris was made by Devliegher et al.(1997). They concluded that nutrient-enrichmentprocesses but not gut associated processes wereresponsible for the increased microbial biomassand activity reported in the presence ofL. terrestris.Meanwhile,endogeicearthwormscan transport freshorganic detritus from the soil surface into burrowswhilemixingitwithmineralsoil.Inthecaseoftropicalendogeic species, it has been demonstrated that theaddition of water and readily assimilable intestinalmucustotheingestedsoilrapidlystimulatesmicrobialactivity. In thesecondhalfof theearthwormgut, themucus will have been almost entirely metabolizedandthemicroorganismsstarttodegradetheSOMintoassimilableOM.ThisformofOMisthenusedbyboththewormsandthemicroorganisms.Furthermore, theinteractionsbetweenearthwormsandmicroorganismsoccuratseveralspatialscalesinthedrilosphere(Brownetal.,2004).Thedrilosphereconcept(Figure 1)wasdevelopedbyBouché(1972),originallytodescribethe2-mm-thickzonearoundtheearthwormburrowwalls.Lavelle(1997)completedthemeaningofdrilospherebyincludingearthwormcommunities, thedigestivetractcontent,andallmicrobialandinvertebratepopulations.Upto60%oftheClossesfromearthwormsduringtheirlife spancanbe in the formofmucus secretion, andthissolubleorganiccarbon isan importantmicrobialstimulantinthedrilosphere(Brownetal.,2004).

Different species differ in their ability to digestorganic residues and assimilate nutrients (Lattaudet al., 1998). Aporrectodea caliginosa earthwormsconsumeamixtureofsoilandOM,oftenchoosingtofeedinpatchesofsoil thatarerelativelyrichinOM,orinmicrositessincetheyareenrichedwithbacteriaand fungi (Wolter et al., 1999).Lavelle et al. (1994)showedthatseveraltemperateearthwormspecieshaveamutualisticdigestivesystem.ThemixtureofsolubleOC,intheformoflow-molecular-weightmucuswithingestedOM, togetherwith themoistconditionsandneutralpHin the foregut,promoted thedevelopmentofamicrobialcommunity thatcoulddigestcelluloseandothersubstancesthatearthwormstypicallycannotdigest. Essentially, the earthworm gut can act like abioreactor where microbial activity and biomass areincreased due to favorable conditions, with readily


availableC,frommucus,andwater.Hence,earthwormcasts(EC)maycontainlargeamountsofOMthathasnotbeenassimilated,butthathasbeenmodifiedbothphysicallyandchemicallyduringpassagethroughtheearthwormgut.TheECareusuallyrichinammonium-nitrogenandpartiallydigestedOM,providingagoodsubstrate for growth of microorganisms. It has beenestablished that thereare largerpopulationsof fungi,bacteria, and actinomycetes (Shaw et al., 1986), andhigher enzymatic activities in EC than in bulk soil(Figure 1).

Earthworms produce a huge amount of intestinalmucus composed of gluco-proteins and smallglucosidicandproteicmolecules(Morris,1985).Themicroorganismsenteringthewormgutsconsumethesenitrogenouscompoundsinmucus(Zhangetal.,2000),which largely increases their activity.The biologicaldecomposition of OM is mediated by a variety ofbiochemical processes inwhich enzymes play a keyrole (Garcia et al., 1992). Themajor constituents ofOM,likecellulose,hemicellulose,lignin,andproteins,are degraded by specific enzymes. Earthwormsfragment the substrate in the process of feeding andtherebyincreasethesurfaceareaforfurthermicrobialcolonization. The enhanced microbial activityaccelerates the decomposition process leading tohumification, thus oxidizing unstable OM into morestable forms. Humification processes are acceleratedand enhanced not only by the fragmentation andsize reduction of the OM, but also by the greatlyincreasedmicrobial activitieswithin the intestinesoftheearthwormsandbytheaerationandturnoveroftheOMthroughearthwormmovementandfeeding.

2.3. Nutrient inputs, mineralization

Earthworms are known to be important regulatorsof major soil processes and functions such as soil

structure, OM decomposition, nutrient cycling,microbial decomposition and activity, and plantproduction. Cortez et al. (2000) reported that thepresence of earthworms whatever the ecologicalcategory, increased the quantity of inorganic N inthesoil.Thiswascausedbyenhancedmineralizationof N forms, both of a 15N-labelled residue and thatof the soil organic matter. Earthworms can impactplant growth by promoting N-availability (Li et al.,2002; Ortiz-Ceballos et al., 2007). Several factorsmay contribute to the mineral weathering mediatedby earthworms, such as low pH and a bacteria-richmicroenvironmentinthegutofearthworms.However,thepresenceofearthwormsmayhaveaneffectontheproductionofgreenhousegasessuchasnitrousoxide(N2O).ResearchbyRizhiyaetal.(2007)indicatedthatearthwormsincreasedN2Ofluxeswhengrassresiduewasappliedtothesoil.TheformationandproductionofN2Oinsoilsisdeterminedbymicrobialprocesses:nitrification,denitrification,andnitrifierdenitrification(Wrage et al., 2001). The earthworm gut providesideal conditions for N2O producing microorganismsby providing abundant substrate, an anaerobicenvironment,suitablepHandahighmoisturecontent(Hornetal.,2003;Drakeetal.,2007).Thepowerfulmechanicalgrindingactionofthegutiscausedbytheperistaltic actions used to move food along the gut,andtheactionofligandsoriginatingfromearthwormsand their gut microorganisms (Carpenter et al.,2007).Earthwormgutsare,consequently,enrichedinmicroorganisms,withconcentrationsmuchhigherthaninthesurroundingenvironment(Carpenteretal.,2007).High numbers of other organisms that are capableof producing N2O (i.e., nitrate-dissimilating andnitrifyingbacteria)arealsopresentintheA. caliginosaearthwormgut(Ihssenetal.,2003).ProductionofN2Obynitrate-dissimilatingbacteriaisfavoredinsystemsthat contain high levels of organic carbon, like the

Figure 1. Diagrammatic illustration of different internal components of the drilosphere, from ingestion to excretion inearthworms(adaptedfromBrownetal.,2000)—Illustration des composantes internes de la drilosphère, de la digestion à l’excrétion chez les vers de terre(d’après Brown et al., 2000).

EARTHWORM INTERNAL

PROCESSESFOREGUT MIDGUT HINDGUT

Exonephridial(external N excretion)

Digestion of fungalhyphae, bacteria,

trophozoites, algae

Intestinal mucus(Assim. C and N)

Antifungal and antibacterial secretions

(antibiotics?) Ammonification(Org. N ➝NH3)

Reassimilation of C

Metabolicwastes

Assoc. N2 fixation(e.g. Chlostridia)?

Bacterial stimulation,Enzyme productionDigestion of organic

compounds

Enteronephridial(N into

the gut)

Tissueproduction(nutrient immob.)

Gizzard(grinding)

Food selectioningestion

Calciferous glands(CaCO, secretion,

pH increase)

Faecesegestion(casts)


rumenor thegastrointestinal tractsofanimals.Somenitrifiers are able to use nitrate or nitrite as electronacceptors and, by using this nitrifier denitrificationsystem, can produce N2O and/or N2 under oxygen-limited conditions (Freitag et al., 1987). The in situconditionsofthegutareidealforactivationofdormantbacteriaandbacterialspores thatmightbepresent insoil.Manyendospore-formingbacillithatareabundantinsoil(Felskeetal.,1998)havebeendetectedinthegutofA. caliginosaspeciesandcanreducenitrateornitritetoN2O(Ihssenetal.,2003).

The increased total nitrogen may be due tothe release of nitrogenous metabolic productsthrough E. eugeniae earthworm excreta, urine, andmucoproteins(Padmavathiammaetal.,2008).Indeed,Dash et al. (1977;1979) reportedhigher levelsofNin casts ofLampito mauritii than in the surroundingsoil. In the gut of earthworms, it is possible that themucus secreted from the gut epithelium provides anenergy source that stimulates biological N-fixation(Lee,1985).

Todeterminetheroleofearthwormsinagrosystemsustainability,itmaybenecessarytofocusonprocessesbywhichearthwormsincreaseordecreasethestorageorlossofnutrients,andhowtheyinfluenceproductivityandnutrientuptakebycrops.Asshowninfigure 2,thepresenceofearthwormscanchangethesizesofvariousnutrientspools,andthefluxesofCandN,significantly(Bohlenetal.,2004a;figure 2).

This model emphasizes the major pathways bywhich earthworms change the retention and loss ofC and N, incorporating the effects of earthwormson soil biological, physical and chemical processes.Throughinteractionsofearthwormswiththemicrobial

community and by processing OM, earthworms canincreasethesystemfluxofCO2(gaseousCloss).Thesesameinteractions,coupledwithearthwormexcretion,canalsoleadtoincreasedavailabilityofN.

2.4. Nutrient dynamics

Earthwormsareimportantdecomposerscontributingtonutrientcyclingprocessesinvolvingnitrogen(Lavelleetal.,1992),phosphorus(Chapuis-Lardyetal.,1998)and carbon (Lee, 1985; Lavelle et al., 1992; Zhanget al., 1995;Curry et al., 2007).They ingestorganicmatter with relatively wide C:N ratios and convertit to earthworm tissues of lower C:N ratios (Syersetal.,1984).Thisacceleratesthecyclingofnutrientsin soil, particularly N. Some field studies indicatethat earthworms feed on organic materials with lowC:N ratio, thereby leaving behind a pool of organicmaterialswithahigherC:Nratio(Bohlenetal.,1997;Ketteringsetal.,1997).

Field studies have shown variable effects ofearthworm invasionon soilNdynamics. Invasionofmaple sugar forests inNewYork byLumbricus spp.increasedleachingofNO3inahistoricallyplowedsite.However,atanothersitethathadneverbeenplowed,the effects have not been observed, which could beattributedtothegreaterpotentialforNimmobilizationin the more C-rich unplowed site (Frelich et al.,2006).Total soilNwasnot significantlychangedbyearthworm invasion (Bohlen et al., 2004b). Duringearthwormfeeding,thenutrients,phosphorus(P)andpotassium(K),areconvertedintoanavailableformforplants.Lavelleetal. (1992)highlight the importanceof earthworm feeding behaviors, which may

contribute to the long-term effectsof earthworms on nutrient cyclingprocesses. Suarez et al. (2004)foundanincreaseinPleachinganddecrease in P availability on plotsin a New York sugar maple forestdominated by Lumbricus rubellus.Sugar maple forests invaded byseveralspeciesincludingL. rubellushadlowerPavailabilitythancontrolparcels without those earthwormspecies (Hale et al., 2005). Loss ofP with earthworm invasion can beassociated with maple decline. Themagnitude of earthworm invasionimpactsonnutrientcyclingdependson the species assemblage ofearthworms that invade as well asland-use history. In order to havesystems of sustainable agriculture,it is important tomaintain a globalbalance of nutrients to ensure that

Figure 2. Ecosystem budgetmodel to examine pools and fluxes ofC andNinthepresenceofearthworms(adaptedfromBohlenetal.,2004a)—Modèle conceptuel comparant les flux du carbone et de l’azote en présence des vers de terre (d’après Bohlen et al., 2004a).

Crop

Root

LitterFertilizer

Runoff

BurrowEarthworm

Microbialbiomass Available

C and NSoil organic

C and N

Matrix and bypass

Stableaggregates

Plant uptake

Gaseous loss


theoutputsandlossofnutrientsareoffsetbynutrientinputs (Giller, 2001). Potassium is one of themajornutrientsforplantgrowththatcansignificantlyaffectthegrowthandproductionofcrops,alongwithNandP(Amtmannetal.,2007;Sugumaranetal.,2007;Chenetal.,2008).HoweverK,intheformofsilicates,canhardlybeusedbyplants(Liuetal.,2006).Earthwormscan help in releasing K from silicate minerals. Forinstance,Baskeretal.(1994)reportedthatexchangeableK-contentincreasedsignificantlyinsoilspopulatedbyearthwormscomparedwithsoilsdevoidofearthworms(Baskeretal.,1992).TheyconcludedthattheincreasewasduetothereleaseofK,fromthenon-exchangeableK-pool, as soil material passed through the wormgut.Somemicroorganisms in the earthwormgut canenhancetheweatheringofmineralsbyloweringpHorby producing ion-complexing organic ligands (Sanz-Montero et al., 2009).EC are usually found to havegreaterexchangeableK,calcium(Ca),andmagnesium(Mg) contents than bulk soil (Edwards et al., 1996;Marianietal.,2007).ThiswasalsoconfirmedbyTengetal.(2012)whoexaminedthephysical,chemicalandbiological properties of casts produced by endogeicspeciesMetaphire tschiliensis tschiliensis inclaysoilincubated in the dark for two weeks. The findingssuggestedimprovednutrientcontentinECascomparedtoWWSandBS(Table 1).Thiswasshownbyhighercontentofmacronutrients(N,Ca)inECthaninbothWWS and BS. This is probably due to the intimatemixing of OM through the earthworm gut whichcan further enhance mineralization and humificationprocesses(Lavelle,1988;Blanchartetal.,1999).

ImprovedCa-contentinECwasprobablyduetothepresenceofanactivecalciferousglandinearthwormsthatactivelysecretesmucusrichincalciumcarbonatesintotheesophagus(Drakeetal.,2007).ThisleadstotheeliminationofexcessCaionsviacastingactivity,andgreatlyincreasesCaavailabilityinsoil.

3. EARTHWORMS AND MICROORGANISMS

The impact of earthworms on soil OM breakdownhas been studied before. However, despite the factthat importanceofsoil fauna inOM-turnover iswellknown,thecomplexinteractionsbetweensoilfaunaandmicroorganisms,andtheindirecteffectsonmicrobialcommunities, are less understood. The biochemicaldecomposition of OM is primarily accomplished bymicroorganisms,butearthwormsarecrucialdriversoftheprocessas theymayaffectmicrobialdecomposeractivitybygrazingdirectlyonmicroorganisms(Monroyetal.,2008;Airaetal.,2009;Gómez-Brandónetal.,2011),andbyincreasingthesurfaceareaavailableformicrobialattackaftercomminutionofOM(Domínguezetal.,2010).Somemicroorganismsmaybea sourceof food for earthworms, but the amounts consumedandtheabilityofearthwormstodigestandassimilatemicrobial biomass vary with earthworm species,its ecologogical category, food substrate, and theenvironmentalconditionsinwhichtheearthwormsareliving(Brownetal.,2004).Earthwormsaffectdirectlythe decomposition of soil through gut-associatedprocesses,via theeffectsof ingestion,digestion,andstimulationoftheOMbreakdownandmicroorganisms(Monroy et al., 2008; Aira et al., 2009). Afterpassage of microorganisms through the earthwormgut (mainly fungal and protozoan spores and someresistantbacteria), theyprovideinoculaformicrobialcolonization of newly formed EC (Brown, 1995).Somebacteriaareactivatedduringpassagethroughthegut,whereasothersremainunaffected,andyetothersare digested in the intestinal tract and thus decreaseinnumber(Pedersenetal.,1993;Drakeetal.,2007).Themicrobialcompositionoftheearthwormintestinecontentshasbeenconsideredtoreflectthatofthesoilingested (Brown, 1995). Furthermore, the numbers,biomass, and activity of microbial communitiesin the earthworm gut have also been shown to bedifferent from that in uningested soil (Schönholzeret al., 1999). Singleton et al. (2003) studied bacteriaassociatedwiththeintestineandcastsofearthwormsand found Pseudomonas, Paenibacillus, Azoarcus,Burkholderia,SpiroplasmandActinobacterium.Someofthesebacteria,suchasPseudomonas alcaligenesandAcidobacterium, areknown todegradehydrocarbons(Johnsenetal.,2005).Monroyetal.(2008)observedareductioninthedensityoftotalcoliformsby98%,afterthepassageofpigslurrythroughthegutoftheepigeicearthworm E. fetida. Accordingly, Pedersen et al.(1993) reported a selective reduction in the coliformEscherichia coliBJ18 in cattledungduringpassagethrough the gut of several species of earthworms ofonegenusLumbricus.Theselectiveeffectsoningestedmicroorganisms through the earthworm gut may becaused by competitive interactions between those

Table 1.Mineralelementsinworm-workedsoil(WWS),earthworm casts (EC) and bulk soil (BS)—Teneurs en éléments minéraux présents dans le sol après ingestion par les vers de terre, dans les déjections des vers de terre et dans le sol témoin en absence de vers de terre(Tengetal.,2012).Elements (mg.kg-1drysoil) WWS EC BSN 2.34 3.78 3.39P 1.11 1.42 1.24K 2.42 2.54 2.48Ca 3.67 5.00 3.92Mg 1.14 1.42 1.16


ingested and the endosymbiotic microrganisms thatreside in thegut (Brownet al., 1981). Indeed,Byzovetal.(2007)foundthatthemid-gutfluidofearthwormspossessaselectivesuppressiveactivitywhilestimulatingcertain soil microorganisms. Meanwhile, Thakuiraet al. (2010) found that food resource type can causeshifts in the gut wall-associated bacterial community,but that themagnitudeof these shiftsdidnotobscurethe delineation between ecological group specificity.Forinstance,sporesofsomefungithatsurvivedinthemid-gut environment (Alternaria alternata) started togerminateandgrewactivelyinfreshexcrement.Thefateofmicroorganismspassing through thedigestive tractofearthworms isan important factor in the formationofthesoilmicrobialcommunityandthedegradationofOM.Recently,Rudietal.(2009)observedarapidandhomogenouschangeinthemicrobiotaingutselectiveeffects on the presence and abundance of ingestedmicroorganisms.These selective effectsmay alter thedecomposition pathways, probably by modifying thecomposition of microbial communities involved indecomposition. Previous studies were mostly aimedto evaluate the effect of gut transit on the microbialpopulation,biomassandenzymeactivitiesofdifferentorganicresidues(Devliegheretal.,1995;Zhangetal.,2000;Scheuetal.,2002;Airaetal.,2006).ButrecentlyAiraetal.(2007a;2007b)showedthatearthwormscanmodifythemicrobialcommunityphysiologyandtriggerenzymeactivitiesduringvermicompostingofpigslurry.Severalenzymesisolatedfromearthwormgutsallowedto digest some bacteria, fungi andmicroinvertebrates(e.g., protozoa, nematodes) (Brown et al., 2000).Studies using 6earthworm species and more than10soil and litter fungal species (Moody etal., 1995;Bonkowski etal., 2000) have shown that earthwormsprefer, and digest, the rapid-growing fungi speciestypically associatedwith theearly successional stagesofdecomposition.

4. EFFECTS OF EARTHWORMS ON SOIL STRUCTURE

The beneficial effects of SOM on soil productivitythrough the supply of plant nutrients, enhancementof cation exchange capacities, and improvements insoilandwaterretentionarewellestablished(Woomeret al., 1994). In addition, SOM supports varioussoil biological processes by acting as a substrate fordecomposerorganismsandecosystemengineers, suchasearthworms.Theyplayaroleinbothaccelerationofdecompositionandmineralizationprocesses(Closs)andincarbonstorageorprotectionfromdecomposition(Caccumulation)instableaggregates(Brownetal.,2000).AggregatestabilityisakeyfactorforphysicalsoilfertilityanditalsoaffectsSOMdynamics(Abivenetal.,2009).

Aggregatesareformedthroughthecombinationofclay,silt,andsand,withorganicandinorganiccompounds.Their stability isusedasan indicatorof soil structure(Sixetal.,2000).Thesize,quantity,andstabilityofsoilaggregates reflect a balance between factors such asorganic amendments, soilmicroorganisms, fauna, anddisruptingfactorsasbioturbationandculture(Sixetal.,2002)(Figure 3).

Aggregation is a complex procedure that includesenvironmental factors, soil management factors,plant influences, and soil properties such as mineralcomposition, texture, SOC-concentration, pedogenicprocesses,microbialactivities,exchangeableions,andmoistureavailability(Kay,1998).Forseveraldecades,the role of soil organisms in soil structure has beenrecognizedbyfarmers,buttheimpactofsoilorganismson the formationof aggregateswas conceptualized inthehierarchicalmodelofsoilaggregatesonlyinthelast25years(Tisdalletal.,1982).Thismodelshowsthattheactivityoffungi,bacteria,plantroots,andmacrofauna(e.g. earthworms) lead to the formation of biologicalmacroaggregates(Sixetal.,2002).Thebreakdownofsoilmacroaggregates increases over time because theactionofbindingagentsisgraduallydisrupted.However,despite the disruptive forces, the microaggregatesremainstableandbecomeblocksduringtheformationof new soil macroaggregates. A study conducted byBossuytetal.(2006)showedthattherewasasignificantinfluenceofearthwormactivityandresidueapplicationon stable aggregate formation. Soil aggregates were4.3timesgreaterthanthecontrol(noearthworms)whenA. caliginosawaspresentinresidues-incorporatedsoils.Further, in thepresenceofL. rubellus, soilaggregateswerethreetimesgreaterthanthecontrol.

Nunan et al. (2003) reported that bacteria are notrandomly distributed throughout the soil; there arevariations in biomass and differential colonizationamong different sizes of aggregates.Usingmolecularmethods,Mummeyetal.(2006)examinedthebacterialcommunities associated with different aggregatesize-fractions in earthworm-worked soil relative tosoilreceivingonlyplant litter.Earthwormsalteredthebacterial community composition in all soil fractionsthat were analyzed. When earthworms ingest thesoil, thesoilparticlesarebrokendownand thesoil iscompacted during passage through the gut prior toexcretion.Barréetal.(2009)reportedthatearthwormswereshowntobringinitiallylooseorcompactedsoiltoanintermediatemechanicalstatethatismorefavorableforstructuralstabilityandrootgrowth.Inaddition,soilsize-distributionissignificantlyaffectedbyearthwormsin the 0–2cm layer of soil (Snyder etal., 2009).Earthwormpresence shifted soil aggregate-size to the>2,000µmfractionfromsmallerfractionsbyreducingtheamountofsoilinthe200–250and250–253µmfractions.


5. EFFECTS OF AGRICULTURAL PRACTICES ON THE DYNAMICS OF EARTHWORM COMMUNITIES

Agricultural practices such as tillage, drainage,irrigation, limeapplication,pesticideuse, fertilizationandcroprotation,caninfluencesignificantlyearthwormbiomassandactivity(Edwardsetal.,1996).Inareviewof several studies exploring the effects of tillage onearthworms, it was concluded that deep ploughingand intensive tilling reduced earthworm populationsinclayloamsoils.Insandyloamstillageeffectswerevariableanddependentuponseveralfactorsincludingtheearthwormspeciespresentinthesoil(Chan,2001).No-till management systems promoted earthwormabundance (Edwards et al., 1996; Johnson-Maynardetal., 2007). However, populations tend to recoverwithinoneyearfromless-severeformsofcultivation,provided the disturbance is not repeated. Whenperformedonceayear,theeffectoftillageonearthwormpopulationswasevenfoundtobelessdestructivethan

that of birds feeding on earthworms. Larger, anecicspecies such as L. terrestris andAporrectodea longawhich require a supply of surface litter and inhabitrelatively permanent burrows, are the species mostadverselyaffectedbyrepeatedsoildisturbance;smallerendogeicspeciessuchasAllolobophora chloroticaandA. caliginosa are less affected and can benefit fromplowed-incropresidues(Lofs-Holmin,1983;Edwards,1984). Eriksen-Hamel et al. (2009) investigated theeffects of tillage on the earthworm Aporrectodea turgidaandsuggestedthatincool,humidagrosystems,tillage-induced disturbance probably has a greaterimpact on earthworm populations and biomass thanfoodavailability.Mechanicalweedingwasfoundtoberesponsibleforhabitatdisturbance,physicaldamagetoearthworms,anddisturbanceinreproductionfunctionsamongotherfactors(Ernstetal.,2009;Peignéetal.,2009).

Agricultural systems are characterized by highlevels of inputs. Biological activity in agriculturalsoils isdrivenbyorganicCinputs. Inputsoforganic

Figure 3.Aggregate formation and degradationmechanisms in temperate and tropical soils—Formation d’agrégats et mécanisme de dégradation des sols(Sixetal.,2002).


materials from crop residue, cover crops, manureapplicationsororganicfertilizershaveastrongpositiveeffectonthecomposition,sizeandactivityofthesoilbiologicalcommunity(Kirchneretal.,1993).Useofsolid materials and organic fertilizers obtained fromplants and animal origins were reported to increaseearthworm populations (Leroy et al., 2007; Leroyet al., 2008; Reinecke et al., 2008). However, mostchemical fertilizers influence earthworms indirectlythrough an increase in plant yield and consequentlyan increase in plant residues that remain in the fieldafter harvest. Earthworms play an important role insurface residue decomposition rate, distribution ofOM throughout the soil profile, and soil physicalpropertymodification.Lowe et al. (2002) found thatOMmanagement is important in thedevelopmentofsustainable earthworm populations and their role insoilameliorationatrestoredsites.AlsotheconversionofgrasslandtoarablelandcanaffecttheSOMandalsodecreaseearthwormpopulations.Indeed,VanEekerenet al. (2008) found a strong decrease in earthwormabundanceafterconversionofgrasslandtoarableland.Onthecontrary,conversionofarablelandtograsslandstimulatedthespeciesrichnessandabundance,eveninthesecondyearafterconversion(VanEekerenetal.,2008).

6. CONCLUSION

Earthworms are important biological factors in soilecosystems.Theyaresensitivetocultivationtechniquesandconsequentlymaybeusedasbioindicatorsofsoilhealth.Earthwormshavebeen suggestedaspotentialindicatorsofthesustainabilityofagriculturalpracticesthat farmers could use, thereby optimizing differentfarming systems. Nevertheless, further researchregarding the impact of cultivation techniques, croprotations,andcropresiduemanagementonearthwormpopulationswithinEuropeisrequired.Also,itwillbeimportanttoexplorethepotentialroleofearthwormsinsoilfertilityandagriculturalsustainability.

List of abbreviations

Al3+:AluminumionsBS:BulksoilCa:CalciumCa2+:CalciumionsC:CarbonEC:EarthwormcastsFe2+:FerionsH:HydrogenK:PotassiumMg:MagnesiumMg2+:Magnesiumions

N:NitrogenN2O:NitrousoxideOC:OrganiccarbonOM:OrganicmatterO:OxygenO2-:OxygenionsP:PhosphorusSOC:SoilorganiccarbonSOM:SoilorganicmatterWWS:Worm-workedsoil

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Impacts of earthworms on soil components and dynamics… · Impacts of earthworms on soil components and dynamics 123 density, as did microbial metabolic activity. In addition, Coq