Population ecology and functioning of insom e arable farming systems

CENTRALE LANDBOUWCATALOGUS

0000 0459 4293 Promotoren: dr. L. Brussaard hoogleraar in de bodembiologie

dr. ir. L.J. Pons emeritus hoogleraar ind e regionale bodemkunde 1 tJtióï'lc } N

Wim Didden

Population ecology and functioning of Enchytraeidae insom e arable farming systems

Proefschrift terverkrijgin gva nd egraa dva n doctor ind elandbouw - enmilieuwetenschappen , opgeza gva nd erecto rmagnificus , dr.H.C .va nde rPlas , inhe topenbaa rt everdedige n opwoensda g8 me i199 1 desnamiddag st evie r uuri nd eAul a vand eLandbouwuniversitei tt eWageningen . BIBLIOTHEEK tÄNDBOUWUNIVERSriEflfr WAGENINGEN

Cover photograph: Wim van Hof ,oüo^io^ |4)M

1. Het belang van potwormenvoo r nutriëntenstromen in (agro)oecosystemen wordt nietallee n bepaald door biomassae n turnover van de populaties, maar tevens door hunvertical everdelin g over het profiel en temporele dynamiek. Dit proefschrift

2. De indirecte effecten van potwormen op de nutriëntenmobilisatie kunnen aanzienlijk zijn als gevolg van de vermoedelijk lage selectiviteit bij de voedselopname en de hoge selectiviteitwaarme evoedse lword tgeassimileerd . Abrahamsen, G.,199 0- Biol .Fertil . Soils 9:159-162 Dit proefschrift

3. Potwormen dragen aanmerkelijk bijaa n de dynamiekva n de bodemstructuur en kunnen zodoende een belangrijke rol spelen bijd e lucht- en vochthuishouding van de bodem. Dit proefschrift

4. De fysisch-chemische parameters die ind e meeste oecologische studies gemeten worden, zijnvoo r hetvoorspelle nva n de aan te treffen hoeveelheden potwormen van geringewaarde . Dit proefschrift

5. Laboratoriumgegevens over de levenscyclusva n dieren zijn slechts dan bruikbaar voorvoorspellinge n van develdsituatie ,wannee r ze tevens bepaald zijn onder daar optredende extreme omstandigheden en wanneer veldmetingen op de relevante schaal worden verricht. Dit proefschrift

6. Ruimtelijke heterogeniteit op micro- en macroschaalvorm t de basisvoo r het functioneren van het bodemoecosysteem en tegelijkertijd een van de belangrijkste hinderpalenvoo r bodembiologisch onderzoek.

7. Het gebruik van functionele groepen inee n oecologische analyse, zonder soort- gericht oecologisch onderzoek naar de in deze groepen geplaatste organismen, leidt onvoldoende tot inzicht in hetfunctionere n van oecosystemen. Hunt,H.W . etal. , 19B7 -Biol . Fertil. Soils 3:57-68 Hetfei tda t oecologischonderzoe k aan potwormen slechts relatief iaat is aangepakt, ondanks hetzee r talrijkvoorkome nva n deze dieren, doet vermoeden dat de ontwikkelingva n de wetenschap medeword t bepaald door angstvoo r het onbekende.

9. De huidige praktijkva n voornamelijk kortlopende contractenvoo r wetenschappelijk onderzoek bevordert zowel de produktiviteit als deverschralin g van dat onderzoek.

10. 'No-nonsense beleid'wijs t niet alleen op een povere beheersing van de Nederlandse taal, maar ook op een duidelijke minachting voor afwijkende meningen.

11. Veel bodembiologisch onderzoek blijft aan de oppervlakte.

Stellingen behorende bij het proefschrift van Wim Didden: Population ecologyand functioningof EnchytraekJae In some arable fanningsystems.

Wageningen, 8 mei 1991 Abstract

Didden,W.A.M. ,199 1- Populatio necolog yan dfunctionin go f Enchytraeids insom e arablefarmin gsystem s• Doctora lthesis , Agricultural University,Wageningen , The Netherlands

Thepopulatio necolog yo f Enchytraeidae,an dthei rfunctioning ,wer estudie di n somearabl efarmin gsystem san di nlaborator yexperiments . Thesystem sstudie d consistedo fa 'conventional ' (highinpu to fenerg yan dmatter ) andsevera l'integrated ' (reducedinpu to fenerg yan dmatter ) systems. Emphasiswa sgive nt opopulatio n dynamicsan dth erol eo f Enchytraeidae innutrien tcyclin gan dsoi lstructur eevolution . Meanyearl yenchytraei dabundanc ean dbiomas si nth esystem sstudie drange d from1100 0ind/m 2t o4300 0ind/m 2, andfro m0.0 8g C/m 2t o0.4 2g C/m 2,respectively . Itwa scalculate dtha t0.5-3.7 %o fth eyearl yorgani ccarbo ninpu twa srespire d byth e enchytraeid populations. Yearlynitroge nflu xfro mth epopulation s (throughstorag ei n enchytraeidtissue ) rangedfro m0.1 9t o0.6 0g/m 2. Therewer en osignifican t differences betweenth esystem sstudie da sregard s populationdynamica lan dproductio necologica lparameters . However,vertica ldistribu ­ tiono fenchytraei d populationsdiffere d markedlybetwee nth econventiona lfiel dan dth e integratedfields ,probabl yrelate dwit hdifference s insoi ltillag ean dth eresultin gdistri ­ butiono forgani cfertilize ran dplan tresidues . Thesedifference s invertica ldistributio n mayhav econsequence sfo rth eris ko f nutrientsleachin gfro mth esystems . Theimpac to fenchytraei d activityo nsoi lstructur eevolutio nwa sstudie d ina fiel d experimentwit hartificia lsoi lcores ,i ncombinatio nwit hfiel dobservations . Itwa sfoun d thatenchytraei dactivit yproduce d measurableeffect s onai rpermeability , poresiz e distribution,an ddistributio n ofaggregat esizes ,probabl ythroug hselectiv eburrowin g andtranspor to f organicbeside s mineralmaterial . Life-history parameterso fEnchytraeus buchholzi, thedominan tspecie sa tth e researchsite ,wer edetermine di na laborator yexperiment ,an dprediction s basedo n thelaborator ytrial swer ecompare dwit hdat ao npopulatio ndevelopmen tunde rmor e naturalconditions . Therewer esignifican tdiscrepancies ,indicatin ga ninfluenc eo fth e physiologicalconditio no fth eexperimenta lanimal so nth elengt ho fth elife-cycl ei nthi s .

Keywords : e- Soi lfaun a- Agro-ecosystem s -Populatio ndynamic s Productionecolog y- Nutrien tcyclin g- Soi lstructur e- Life-history Contents

1. General introduction 1

1.1. Outlineo fthi sthesi s 5

2. Ecologyo fterrestria lEnchytraeida e 7

2.1. Introduction 7 2.2. Factorsinfluencin g populationsize so fEnchytraeida e 8 2.2.1. Introduction 8 2.2.2. Abioticfactor s 12 2.2.2.1. Moisture 12 2.2.2.2. Temperature 13 2.2.2.3. pH 14 2.2.3. Bioticfactor s 15 2.2.3.1. Foodan dfeedin g 15 2.2.3.2. Competition 17 2.2.3.3. Predatorsan dparasite s 18 2.2.4. Maninduce dfactor s 20 2.2.4.1. Physicalhabita tchange s 20 2.2.4.2. Chemicals 21 2.2.4.2.1. Pesticides 21 2.2.4.2.2. Fertilizers 24 2.2.4.2.3. Pollution 25 2.3. Therol eo f Enchytraeidae inecosyste mfunctionin g 27 2.3.1. Introduction 27 2.3.2. Soilstructur e 27 2.3.3. Microdistribution of Enchytraeidae 28 2.3.4. Populationdynamic s 29 2.3.5. Production ecology 31 2.4. Concluding remarks 35 3. Populationdynamic san d productionecolog yo f Enchytraeidae inhig han dreduce dinpu tfarmin gsystem s 36

3.1. Introduction 36 3.2. Methodsan dmaterial s 37 3.2.1. Theexperimenta lsit e 37 3.2.2. Sampling procedure 38 3.2.3. Analysiso fth edat a 39 3.2.4. Productionecologica lcalculation s 39 3.3. Results 41 3.3.1. Compositiono fth eenchytraei dfaun a 41 3.3.2. Verticaldistributio nan drelatio nt oplan tpositio n 42 3.3.3. Thecanonica lcorrespondenc eanalyse s 44 3.3.4. Relationsbetwee nbod yweigh tan dlengt h 46 3.3.5. Population dynamics 46 3.3.6. Respirationan dproductio n 49 3.3.7. Nitrogenturnove r 50 3.4. Discussion 52

4. Life-history ofEnchytraeus buchholziVejdovsky ,187 9 ()an dpopulatio ndevelopmen t inartificia lsoi l 57

4.1. Introduction 57 4.2. Methods 58 4.2.1. Life-history characteristics 58 4.2.2. Population development inartificia lsoi lcore s 59 4.2.3. Themode lfo rpotentia lpopulatio ndevelopmen t 59 4.3. Results 60 4.3.1. Life-history characteristics 60 4.3.2. Growthrate s 62 4.3.3. Comparisono f modelprediction swit hdat afro martificia lcore s 62 4.4. Discussion 66 4.4.1. Comparisono fth epresen tdat awit hothe rlife-histor y studies 66 4.4.2. Evaluationo fth epresen tlife-histor ydat a 67 4.4.3. Synthesis 70 5. Ametho dt oconstruc tartificia lsoi lcore sfro mfiel dsoi lwit h a reproduciblestructur e 72 Agriculture, Ecosystems and Environment, 34 (1991):329-333

5.1. Introduction 72 5.2. Descriptiono fth emetho d 73 5.3. Practicalconsideration s 74 5.4. Results 75 5.5. Discussion 75

6. Involvement ofEnchytraeida e(Oligochaeta )i nsoi lstructur e evolutioni nagricultura lfield s 76 Biology and Fertility ofSoils ,9 (1990) :152-15 8

6.1. Introduction 76 6.2. Methodsan dmaterial s 77 6.2.1. Theexperimenta lfiel d 77 6.2.2. Thefiel dsamplin g 78 6.2.3. Thefiel dexperimen t 78 6.2.4. Treatments infiel dexperimen t 80 6.3. Results 81 6.3.1. Thefiel dsamplin g 81 6.3.2. Thefiel dexperimen t 83 6.4. Discussion 88

7. Synthesis 90

8. Summary 94

9. Samenvatting 98

10. References 102 Woordvoora f

Toeni ki n198 6bego nme the tbestudere nva nd eoecologi eva n potwormen, wist iknauwelijk swa tpotworme nware ne nwelk evrage no pdi tterrei n liggen. Nu,vij fjaa r later,be ni ke rmi jdaa ri niede rgeva lbete rva nbewust . Ditproefschrif t vormtd eneer ­ slagva ndi tleerproces . Hoewelslecht sbi jéé nhoofdstu kva ndi tproefschrif t anderenzij ngenoem dal s mede-auteur, houdtda tgeenszin si nda talle so peige nkrach ti sgedaan . Zonderd e steun,aanmoedigin g enkritie kva nvelen ,zo udi tproefschrif t erwaarschijnlij k nietzij n geweest. Opd eeerst e plaatswi li khie rmij nouder sbedanken ,di emi jsteed shebbe n aangemoedigdo mmij ninteresse st evolgen ,e nspeciaa l mijnvader ,di emi ja lvroe gi n contactbrach tme td enatuu re nmi jleerd ekijke ne nluisteren . Helaasheef thi jnie t meermoge nmeemake nwa tdaarui ti svoortgekomen . Lijbert Brussaard heeft,doo rd evel estimulerend e gesprekkene ndiscussie sove r hetonderzoe k zelf enhe tbeschrijve nervan ,ee nhee lbelangrijk ero lgespeel d bijd e totstandkomingva ndi t proefschrift. LeenPons ,hoewe lnie tvaa kaanwezig ,heef tdoo r zijnonbevange nkij ko pd eproblematie k mijdez esom svanui tee nande rperspectie f latenzien . Tweemense ni nmij ndirect ewerkomgevin g zijnsteed shee lbelangrijk ,e nvaa k onmisbaargewees tgedurend ed eafgelope njaren . JokeMarinisse nheeft , inonz e tallozediscussie s overon sbeide ronderzoek ,ee nzee rbelangrijk epositiev ero l gespeeld,e nRijnder td eFluite r heeftme tvee lgedul de ninze ttalloz e klussengeklaard , vanhe ttelle nva npotwormeiere nto the ti nwee re n windbemonstere no pd eLovink - hoeve. Jokee nRijndert ,bedankt ! Demedewerker s inhe tLovinkhoeve-project , metnam ePete rd eRuiter ,Gerri t Lebbink, Lucas Bouwmane nRiek sva n Faassen,e nt évee landere no mhie ro pt e kunnennoemen ,wi li kbedanke nvoo rd ecollegial esamenwerkin g end esom shevige , maaraltij dvruchtbar ediscussies . Opd eLovinkhoev ezel fware nd ehere nKonin ge n Danielsdegene ndi ee rvoo rzorgde nda the tonderzoe k überhaupt mogelijkwas , waar­ vooro pdez eplaat s mijndank . DankzijJo s Kroesbergen kondend egrot ehoeveelhede n kunstmatigebodem sdi e voord eexperimente n nodigwaren ,worde ngeproduceerd . Bovendien speeldehi jee n belangrijkero lbi jd eontwikkelin gva nd emethod evoo rhe tvervaardige nva ndez e bodemse nwa shi joo kdegen edi emi jeni gbegri pvoo rbodemfysisch ebepalinge nwis t bijt ebrengen . Zonderd ehul pva nMaj aKooistr azo ui knie ti nstaa tzij ngewees to mee nbegi nt e maken methe tbestudere nva nd epolijstblokken ,e noo khaa rinbren gi nd ediscussie s overd einvloe dva npotworme n opstructuurontwikkelin g isvoo r mijbelangrij kgeweest . Cajote rBraa kwi li khierbi jbedanke nvoo rhe tfei tda thi jmi jenigermat ewegwij s heeftwete nt emake ni nd etoepassin gva ncanonisch ecorrespondentieanalys e opmij n soortgegevens ,e nvoo rzij nkritisch ekanttekeninge n bijd emanie rwaaro p ikd eresul ­ tatendaarva npresenteerde . Menzo umij nsoor twer k kunnenbeschouwe n alsee nvreemd eeen di nd ebij tva n devakgroe pBodemkund ee nGeologie . Tochhebbe nmij ncollega' so pdez evakgroe p mijnooi the tgevoe lgegeve nda tzi jda tz oervoeren . Metnam ewi li khierbi j Nicova n Breemenbedanken ,di ei nstaa twa som ,ondank szij novervoll eprogramma , regelma­ tigech taandach tvoo rmij nwer kt ehebben . Praktischeprobleme n blekeni nd epraktij k zeldenproblemen ,dankzi jd einze te nmedewerkin gva nvee lvakgroepsmedewerker s onderwi eFr éSchelbergen ,Norber t Lukkezen,Marce lLubbers ,Marja n Noordhoek, JokeCobbe ne nvel eanderen . Specialevermeldin gverdiene n demedewerker sva n hetchemisc hlaboratorium ,zonde rwi eee nbelangrij k deelva nhe twer knie tgeklaar d zouzijn . BedanktTin iva n Mensvoort, EefVelthorst ,Le oBegheyn ,Fran sLettink ,Nee l Nakkene nElle n Burger! Hoewelnie ti ndi tproefschrif t terugt evinden ,heef the twer ko phe tvoormalig e ITALee nflin kdee lva nd etij dbeslagen . Hierbijwi li kd emedewerker sva nd eafdelin g bodembiologie,me tnam eGij sSchelling ,Pete r Kuikmane nHan sva nVee nbedanke n voor hungastvrijhei de nhulp . Iwoul dlik et othan kBen tChristense n inCopenhage nfo rintroducin g met o'th e worldo fenchytraeids' ,an dlearnin g meno tt odespai rwhe nlookin gfo ra spermathec a ina movin gan dwrigglin gmas so fcells . Tenslottedan ki kElle ne nMijntje ,die ,hoewe lda tnie taltij deve ngemakkelij kwas , mija ldi etij dhebbe n gesteund. I.Generalintroductio n

Although mani nWester n Europeha sworke dth esoi lfo rthousand so fyears ,soi l itself,an dth eprocesse s responsiblefo r itsfertility ,have ,til lfairl yrecently ,alway sbee n treateda sa blac kbox . Managementpractice stherefor eseldo minclude dconsciou s manipulationo fsoi lprocesse so rbiot aa sa mean so fincreasin g production. Thus, althoughmeasure s liketillage ,cro protatio nan dmanurin gprove dsuccessful , the underlyingmechanism sremaine d unknown. Itwa sno tunti lth e 19,hcentury ,tha tscien ­ tificknowledg eo fsoi lchemistr yand ,t oa lesse rextent ,soi lbiolog ystarte dt odevelop , withth ediscover y ofchemica lfertilizatio n (VonLiebig ,1840 )an dth ewor ko fDar ­ win (1881)o nearthworms . Theus eo finorgani cfertilizer s permitted intensificationan d expansiono fagricultura lpractice ,a proces swhic hwa sstimulate d byth eincrease dus e ofchemica lpesticide ssinc eWorl dWa r II. Forsom etime ,agronomist s generally believedtha ta combinatio no f mechanicalan dchemica lmanagemen t practices en­ ableda continuin g expansion,wit hth emaintenanc eo fsoi lfertilit yan dstructure ,an d controlo f pestsan ddiseases . Inmos ttype so fagriculture ,soi lbiot a(microorganism s andespeciall yanimals ,wit hth eexceptio no fearthworms ) werelargel yignored ,unles s theywer esuspecte d ofbein ginjuriou st ocrop so ranimals . Economicallyspeaking , thisha sbee na successfu lapproach .

Inrecen tyears ,however ,th epric etha twa spai dfo rth eeconomi csucces so fthi s typeo fagricultur e becameincreasingl yclear ,fro m problemswit hsoi lfertilit yan dth e environment. Urgentproblem s inthi srespec tare : - Pollutiono fgroundwater ,surfac ewate ran datmosphere ,cause db yth eintensiv e andinefficien t useo finorgani cfertilizer s andmanure sleadin gt oleachin gand/o r volatilization ofexces samounts . Parto fth e'aci drain ' problemoriginate sfro m theseprocesses . - Environmentalside-effect s ofpesticides ,tha tar ebein guse dabundantl yan da t highcost s (bothfinanciall y andpublicly) . - Deterioration ofsoi lstructur ei nman yagricultura lsoils ,cause db ya decreas ei n soilorgani cmatte rthroug hcro protation sincludin g moreroo tcrops ,an db yth e useo f heavymachiner yunde rto owe tconditions . Asconsequences ,problem s withwate r infiltration,workabilit yan dtrafficabilit y mayoccu r inman ysoils ,leadin g toth enee dfo reve nmor eintensiv etillage . Moreover,throug hdeterioratio n ofsoi l structurean denlargemen to fagricultura lfields ,erosio n problemsma yoccur .

Theseproblem sstimulate dth einteres ti necologicall ysoun dform so f landuse ,i n whichmanagemen t practicesar etune dt oenvironmenta lan deconomica lobjectives . Suchform so f 'integrated'lan dus eimpl yreduction so fmechanica lan dchemica linput s toth esystem ,an yyiel dreductio nt ob ebalance d byth ereductio no fcosts . Animpor ­ tantconditio n inthi s respect is, thatth eus eefficienc y ofexogenou s inputswil lb e increasedb ymakin gus eo f naturallyoccurring ,interna lprocesse so f soilstructur e evolutionan do fstorag ean dtransformatio no f plantnutrients . Athoroug h knowledgeo f thesemechanism s notonl yrequire sa nunderstandin g ofphysica lan dchemica lproc ­ essesoccurrin gi nth esoil ,bu tals oo fth ebiologica lprocesses ,a smicrobia lan dfauna l activities becomemor eimportan twit hreductio no f humaninputs . Soilstructur ei sbein gbiologicall y affectedthroug h microbialan d biochemical processestha tcontribut et oth eformatio n ofsoi laggregate san dinfluenc ethei rstabilit y (Oades,1984) . Ona different , butno tles simportan tscale ,soi lstructur ei saffecte d throughth econstructio n anddisruptio no fmor eo rles sstabl echannel san dvoid sb y theactivit yo f rootsan dsoi lanimals ,an db yth emixin go forgani can d mineralmateria l byfauna lactivit y (Tischler, 1965;Wallwork , 1976;Coleman ,1985) .

Figure 1.1: Schematicdiagram ofthe flows ofmatter in thedecomposition subsystem, and major regulatory interactions. Boxesrepresent pools ofnutrients. Solidarrows represent flowsof matter, dashed arrowsregulatory interactions. DOM= Dead organic matter; MS =Microbial saprovores; AS = saprovores; M= Microbivores; P= Predators; MIN = Mineralized nutrientspool. Soilfertilit y isver yclearl y biologically affected,a sdecompositio n oforgani cmate ­ rial, botho f upper-an dundergroun dorigin ,i sfo rth elarge r parta biologica l process,i n whichmicro-organisms ,an dmeso -an dmacrofaun aar eintimatel y involved,i nway s thatar eonl ygraduall ybein gdisclosed . Figure1. 1 isa schemati cdiagra mo fth e de­ composition subsystem,representin gth eoveral lprocesse stakin g placei nth edecom ­ position oforgani c material. Solidarrow si nth ediagra m representflow so f matter, dashedarrow s importantregulator y mechanisms. Partlydecompose d materialan d deadmicrobia lan danima ltissu ereturn st oth epoo lo fdea dorgani cmatte r (DOM),an d mayb eprocesse dove ran dove ragai nbefor ei ti scompletel y respiredo rotherwis e mineralized,o rtransforme dt orelativel ystabl ehumus . Thisrecyclin go f matterdistin ­ guishesth edecompositio n subsystemfro mth eherbivor esubsystem ,wher eth e re­ mainso forganisms ,onc edea do rconsumed ,leav eth esubsyste ma sdea dorgani c material,thereb yenterin gth edecompositio n subsystem (Heal& MacLean ,1975) . Thedecompositio n ofa particula r pieceo fdea dorgani c matterstart swit hth e colonization bymicrobia lsaprovore s (MS),rapidl ydecomposin geasil ydegradabl e organiccompound s (mostlyth esimple rcarbohydrates) . Thisproces si senhance db y saprovorous (AS)comminutin gth emateria lan dthereb yenlargin gth esurface s thatar ecapabl eo f beingcolonized ,an db yeffect s ofgrazin g bymicrobivorou sanimal s (M)o nmicro-organisms . Grazing,thoug hreducin g microbial biomass,ma yals o stimu­ latemicrobia lactivity ,preven tagein go fcolonie sand ,i fselective ,ma yinfluenc eth e microbialcommunit y structure. Faunalactivit y mayals ob eimportan t intha tanimal s mayac ta svector s inth epropagatio no fmicro-organisms . Inthes eway smobilizatio n ofnutrient s mayb eincrease d orreduce db yth eactivitie so fth esoi lfaun a (Mooree tal. , 1988). Laterstage s ofdecompositio n arecharacterize d bya slowin g downo fth eprocesses ,whe nth eproportio no f morerecalcitran tcompound sincreases . Thisrelativel ysimpl epictur eo fth edecompositio n process isi nrealit ymuc hmor e complex,a sa consequenc eo fa variet yo ffactors : - Thesoi lcommunit y hasa structur ewit hsevera ltrophi cpositions ,i nwhic heac h groupo forganism si sbein ginfluence d bysevera lothers . - Iti sno tunusua ltha ton especie sbelong st osevera ltrophi cposition sa tth esam e time,exhibitin gdifferen t degreeso fomnivory ,o rshow sa tempora lshif t infeedin g habits,a swit hpredator stha t insom eperiod s maychang ethei r habitst osapro - voryo rherbivory . Directlyrelate dt oorgani c matterdecompositio n isth efac ttha t manysoi lanimal s mayb eregarde da ssaprovore s aswel la smicrobivores , be­ causevirtuall y allorgani cmatte rtha ti sconsume di nsoi lcontain s microbialcolo ­ nies. - Normally,al lstage so fdecompositio n occurtogethe r inth edecompose rsubsys ­ tem,an dth e numberan dtype so fstage swil ldiffe r pertyp eo fsubstrate . Hence, thesoi lsyste mi scharacterize d byth espatia lan dtempora lcoexistenc e of numer­ oustype so f microhabitats,differin g inintensit yo fth edecompositio n processes occurring. Moreover,th esiz eo f microhabitatsa sexperience db ysoi lorganism s willb erelate dwit hthei row nsiz ean dactivity .

Itwil lb eclear ,tha ti nman ycase si ti sdifficul tt oasses sth erol etha t anorganism , ora grou po forganisms ,play si nthi scomple xsystem . Thesedifficultie s areth e greatersinc emos tdecompositio n processesoccu ri nmicrosite s insoil ,tha tar egener ­ allyno taccessibl et odirec tobservations . Yet,fo ra nincreasin gnumbe r oforganisms , their parti sgraduall y becomingclearer ,a smore ,an dmor ecoordinate d researchi s beingdevote dt othei rstudy ,an dbette rmethod so fresearc han danalysi sar ebein g developed.

Fora lon gtim e Enchytraeidae (potworms) havelargel y beenignore d inthi styp e of research,bot hi nnatura lan dagricultura lsystems ,fo ra variet yo f reasons. Asregard s agroecosystems,th ereaso nfo rneglectin genchytraeid swa sth esam ea sfo rothe rsoi l organismsan despeciall y soilfauna :the ywer esimpl ydeeme dunimportant . Oneo fth e firstoccasion sthe yattracte dattentio ni nagricultura l respect,wa swhe nthe ywer e thoughtt ob epossibl yinjuriou st osuga rbee t (Vejdovsky, 1892;Stoklasa ,1897) . The mostimportan treason sfo rno tconductin g researcho npotworms ,however ,wer eo fa morepractica lnature :difficultie swit hthei rextractio nfro msoil ,an despeciall ysystem ­ atican dtaxonomi edifficulties . SinceO'Conno r(1955 )develope d arelativel ysimpl e andreliabl eextractio nmethod ,an dth etaxonom yo f Enchytraeidaewa srevise db y Nielsen& Christense n (1959,1961,1963),a nincreasin gamoun to fstudie s havebee n carriedout ,notabl yi nnatura lhabitats ,an dknowledg eo nth eecolog yo fthes eanimal s isgrowing . Itha srepeatedl ybee ndemonstrate d sincethen ,tha tenchytraeid sma y constitutea majo relemen to fth esoi lfauna lcommunit y ina variet yo f habitats,als oi n arablefields ,i ntemperat eregions . Asstil lrelativel y littlei sknow nabou tth efunctionin go f enchytraeids inecosys ­ tems,an dmos tknowledg eoriginate sfro mmor eo rles snatura lhabitats ,a nagricultur ­ allyoriente dresearc hprojec taddressin gthi sfiel dha st odea lwit ha variet yo ffunda ­ mentalquestions . Theseissue sinclud epopulatio n dynamics,specie scomposition , energeticalsignificance ,reproductiv e potential,ecologica lefficiencies ,foo dprefer ­ ences,reaction st oxenobioti c substances,behaviou r insoi letc . 1.1.Outlin eo fthi sthesi s

Fromth ever ybeginning ,th eresearc hreporte di nthi sthesi swa sembedde di n the Dutch Programmeo nSoi lEcolog yo fArabl e FarmingSystems ,a nintegrate dmultidis - ciplinaryresearc h programmewhic hfocusse so nth efunctionin g ofdifferentl ymanage d agroecosystems. Agenera loutlin eo fthi sprogramm ewa spresente db y Brussaard etal . (1988). Themai nobjectiv ei st ogenerat escientifi c knowledgerele ­ vantfo rth epractic eo f sustainable ('integrated')arabl efarming . Researchi sbein g carriedou to nth eexperimenta lfar m'Dr . H.J.Lovinkhoeve 'i nth e Noordoostpolder, reclaimedfro mth ese ai n1942 . Here,experimenta lfield shav ebee nlai dout ,tha thav e conventionalan dvariou stype so fintegrate dmanagement . Inconcordanc ewit hth e generalproblem si nagricultur ementione dabove ,th emai nresearc htheme sare : 1. Theflow so fcarbo nan dnitroge ni nth esystem san dth emechanism sinvolved . 2. Theinteraction s betweensoi lorganism san dsoi lstructure .

Theresearc ho nEnchytraeida estarte dou twit htw oderive dquestions : 1. Whatd oenchytraeid s contributet osoi lstructur eevolutio ni nagricultura lfields ? 2. Whati sth esignificanc eo fenchytraei dpopulation s inagricultura lfield sconcernin g decomposition oforgani cmatte ran dnutrien tdynamics ?

Fromth ebeginning ,i twa sclea rtha tt ounderstan dth epar tplaye db yenchytraeid s inth efield sunde rstud yi nan yquantitativ eway ,i twa snecessar yt oconduc ta popula­ tiondynamica lstudy . Invie wo fth erelativel yscarc eecologica lknowledg eo npot - worms (chapter 2),i twa sdecide dno tt orel yo nth efe wavailabl edat ao nenchytraei d populations inarabl efields ,bu tt ocarr you ta detaile dsamplin g programme. Thisstud y yieldeddat ao nnumber san dbiomas so fenchytraeids ,an dthei r seasonaldynamics , ando nspecie scomposition ,phenolog yo fth epopulations ,an ddept hdistribution s (chapter3) . Theresult so fth epopulatio ndynamica lstud ywer euse dt ocalculat eproductio n biologicalparameter ssuc ha srespiration ,productio nan dconsumptio no fth e enchytraeids,an dt oestimat eth eamoun to f nitrogentransforme ddirectl yb y enchytraeids (chapter3) . Thereproductiv e potentialo fa specie si sa nimportan tfundamenta laspec to f enchytraeidbiolog ytha tha st ob eunderstoo dt ob eabl et opredic tpopulatio ndevelop ­ ment,an dt oinclud e knowledgeo fenchytraei dpopulatio n biologyi nsimulatio nmodels . Ina serie so flaborator yexperiments ,th elife-histor yo fEnchytraeus buchholzi, the dominantspecie sa tth eLovinkhoev eexperimenta lsite ,wa sstudied . Theresult so f theseexperiment swer euse dt opredic t populationdevelopmen t underfiel dconditions , andthes eprediction swer ecompare dwit hactua lpopulatio ndevelopment . These experiments aredescribe di nchapte r4 . Chapter5 deal swit hth edevelopmen to fa metho dt oconstruc tartificia lsoi lcores , usedi nexperiment s onth einteraction s of potwormsan dsoi lstructure . Suchartificia l soilswer econsidere da prerequisit efo ra meaningfu lstud yo finteractions ,a sthe y combinea reproducibl esoi lstructur ewit ha near-natura lenvironmen tfo rth e experi­ mental animals. Inth eexperiment s onth einteraction s betweenenchytraeid san dsoi lstructure ,no t theeffect so f soilstructur eo npotworms ,bu tonl yth eeffect s ofpotworm so nsoi lstruc ­ tureevolutio nwer estudied ,a sthi swa sconsidere dth emos tinterestin g problemi nth e fields understudy . Anexperimen twa scarrie dou ti nwhic hartificia lsoi lcores ,wit han d withoutpotworms ,an dwit han dwithou tadde dorgani cmaterial ,wer ebrough tint oth e field. After retrievalth ecore swer eanalyze d invariou sway st oquantif yenchytraei d effects onsoi lstructur e (chapter6) . Thethesi s isconclude dwit ha synthesi s (chapter7) . 2. Ecologyo fterrestria l Enchytraeidae

Abstract

Thusfar ,littl e isknow nabou tth epar tenchytraeid s playi necosystems ,bot h naturalan dmanaged . Inthi s reviewo fth eecologica lliteratur ei ti s shown, that,althoug h iti sclea rtha tenchytraeid s mustconstitut ea nimportan tfauna l groupi nth esoi lo fman yterrestria lecosystems ,thei r parti sdifficul tt o quan­ tify becauseo f scantyknowledg eo fth efactor sinfluencin gpopulatio ndynam ­ icsan dactivity . Thisi sbecaus emos tstudie shav eno tbee ncarrie dou ta t thespecie slevel ,whil e iti sclea rtha tther eexis tappreciabl e interspecific differences asregard sbiolog yan d responset oenvironmenta lfactors .

2.1. Introduction

Nowadays,muc hecologica l research isaime da tth e revealmento f structuresan d processesoccurrin gwithi necosystems ,i nterm so fpool san d flowso fenerg yan d matter. Notablyi n researchproject saime da tth e developmento fsustainabl eagriculture ,th enee d forsuc hinformatio n isclearl yfel t (Andren,1988 ;Brussaar de tal. , 1988). Inthi styp eo f research, increasing use is being made of simulation modelling, that may help to understand,an deventuall yinterven eintelligentl yi nth efunctionin go fecosystems . Inmost simulatio nmodel stha tincorporat efauna lelements ,parameter slik edat ao nth elife-histor y ofspecies ,thei rfoo dpreferences ,an dreaction st oabioti cfactor spla ya n importantpart . Particularly in the case of soil fauna, however, it often appears to bedifficul t toobtai n reliable estimates of such parameters. Especially as regards Enchytraeidae, available dataar escarc ean d oftenhar dt ofind . Thepurpos eo fth epresen trevie wi st ogathe rth e available knowledge in this area, and to identify topics where more study is needed. Besides,i ti sattempte dt ogiv ea nimpressio no fth e relativeimportanc eo fenchytraeid si n terrestrial ecosystems. Thescop e of this reviewwil l therefore comprise the ecological aspects ofenchytraei dbiolog yan dth edynamic san dfunctionin go fenchytraei dpopula ­ tions. Extraattentio n will begive n to man-induced influences andt oth efunctionin g of Enchytraeidae interrestria lecosystems . Intw oearlie r reviews,O'Conno r(1967,1971 )summarize dth eavailabl eknowledg e onth e ecologyo fterrestria lEnchytraeidae . Due toa nincreasin ginteres ti nthei rimportan t rolei nsoi lprocesses ,includin gnutrien tcycling ,man ymor estudie shav ebee ncarrie dou t since then. Kasprzak (1982) examined more recent literature on enchytraeid ecology, restricted toagroecosystems . Inth etw osurvey s byDas h (1983,1990) onenchytraei d biology,th escop ewa sto obroa dt ocove renchytraei decolog yi nan ydetail . Invie wo fth e increased quantity of data, a review of recent advances in enchytraeid ecology would thereforesee mappropriate . It would be too far-reaching to include systematics and in the present review. Muchi nthes efield sha schange d sinceth ewor ko fNielse n& Christense n(1959 , 1961,1963),an di ti sclea rtha ti nvie wo fth evita limportanc eo fsystematic san dtaxonom y formos tecologica lstudies , ofth eman yne wspecie sdescribed , ando fnewl ydevelopin g insightsan dmethodologies ,ther ei sa nee dfo ra revie wo fth eadvance si nthes efields ,too .

2.2.Factor s influencing populationsize so fEnchytraeida e

2.2.1. Introduction

TerrestrialEnchytraeida ehav ebee nrecorde dfro mal lcontinents . Thehabitat sthe y populaterang efro mglacier st otropica lrai nforest san dfro msavanna st omoors . Althoughnumerou sauthor sreporte do nth eoccurrenc eo fenchytraeids ,mos trecord s originatefro m incidental samples orfaunisti c surveys (e.g.Backlund , 1945;Nurminen , 1965a; 1965b; 1967b; 1970;1973a,b,c,d,e ; Healy, 1979; 1980a,b). Such data,thoug h often worthwhile alsofro m an ecological point ofview , typically are obtained fromfe w samples per locality, taken during a restricted time, and, more often than not, using qualitativeextractio n methods. Density estimatesfoun d inthi swa yca nno tb euse dt o characterize enchytraeid abundances in various habitats, since the estimates are not reliablean dth eeffec to f populationdynamic sar eno ttake nint oaccount . Forthis ,mor e scarcely gathered census data are needed, based on year-round sampling in well documentedsites ,an dusin greliabl equantitativ eextractio nmethod slik ethos edescribe d byNielse n(1953 ;1955a) , O'Connor(1955,1962 )an dSchauerman n(1983) . Application ofthes ecriteri at oth eavailabl eliteratur edat aexclude ssom eotherwis evaluabl estudie s likethos eo fAbrahamse n(1972) ,Solhu y (1975)an dParmele e(1987) ,bu ta fairl ylarg e number of data remains, recorded inTabl e 2.1. In this table,th e mean abundance of enchytraeids,calculate do nth ebasi so fregula rsamplings ,i sliste dfo ra numbe ro fsites , together with some abiotic characteristics. The depth of sampling varied between the variousstudie si nthi stable ,bu ta sth esamplin gdept hgenerall ywa si naccordanc ewit h thevertica ldistributio no fth epopulations ,thes edensit yestimate sma yb e compared. InFigur e2. 1th eabundanc edat afro mTabl e2. 1ar eplotte dagains tth e environ­ mentalvariables . Generally,n ocorrelatio n seemst oexis tbetwee nenchytraei ddensi ­ tieso nth eon ehand ,an dmea nannua lprecipitation ,mea nannua ltemperature ,an d acidityo fth esoi lo nth eother . Largestpopulation s havebee nfoun di ncol dt otemper ­ ate,mois thabitats ,bu tthi sma yals ob erelate dwit hth egreate ramoun to fdat afro m thisregio no fth eworld ,especiall yfro mEurope . Withth eexceptio no fth edat afro mYeate s (1968)an dthi sthesis ,al lsite s listedi n Table 2.1 havea p H valuebelo w7 . Thissuggest stha tenchytraeid sar emainl yfoun d inneutra lt oaci dsoils ;however , Healy(1980a) ,amon gothers ,ha srecorde dsubstan ­ tialpopulation so fpotworm sfro mmor ealkalin esites ,bu tther ear en odat ao npopula ­ tiondynamic s inthes ehabitats . Thelarg evariabilit y ofth edat ai sconspicuous . Whileth elarges tmea n abun­ dances havebee nrecorde dfro m moors(Peachey , 1963),mois tconiferou sforest s (Kitazawa,1977 )an ddun egrasslan d (Yeates,1968) ,lowes tdensitie sals ower efoun d inmoist ,temperat e habitats (Dash& Cragg ,1972a ;Nakamura ,1980) . Thisconsider ­ ablevariabilit y suggeststha tth especie scompositio no fenchytraei dcommunities ,an d thephysiologica l andbehaviora ladaptation so fth evariou sspecie s mayb eimportan t aspects. Unfortunately, inth emajorit yo f populationdynamica lstudie so n

Table 2.V.Average abundanceand environmentalcorrelates of Enchytraeidae in various habitats. Sampledepths assumedsufficient to yield the major part ofthe populations.

Biotope Country Precipitation Air temperature pH Abundance Author (mm/year) (Ann. mean, 'C) Number/m*)

Grassland

Onobrychido-Brometiim Germany (GDR) 550 8.0 13500 Dünger, 1978 idem, forma typicum Germany (GDR) 550 8.0 10700 Epipactis-Seslerietum Germany (GDR) 550 8.0 2700 Festuca rubra Germany (FRG) 1045 6.6 40000 Ellenberg et al., 1986 Dryas site Norway 850 -1.4 3400 Klungland, 1981 on limestone England 780 5.6 5.0-5.8 80000 Coulson&Whiflaker,1978 Nardus England 780 5.6 4.8-5.0 120000 Ammophilaarenari a dune New Zealand 7.5-8.6 130000 Yeates, 1968 raised beach Canada 185 -14.9 7.8 9000 Ryan,1977 sedge-moss meadow Canada 185 -14.9 6.5 27500 sedge meadows Alaska 170 -12.2 4.9-5.4 46100 Maclean, 1980 alpineherbfiek J Australia 2160 3.3 4.3-4.9 3250 Wood, 1971 tropical India 1150 29.8 6.6 3800 Thambi& Dash, 1973 natural Canada 341 3.6 7.5 30000 Willard, 1974a irrigated Canada 341 3.6 7.5 39000 unused hay-land Germany (GDR) 710 9.1 4.5 49000 Brockmann, 1984 abandonedfiel d Sweden 518 5.4 5.8-6.5 23800 Persson & Lohm, 1977 grazed, 10sheep/h a Australia 750 14.3 5.6 6000 King & Hutchinson, 1976 grazed, 20sheep/h a Australia 750 14.3 5.5 2600 grazed,3 0 sheep/ha Australia 750 14.3 5.6 2300 grazed Japan 1200 7.8 1650 Nakamura, 1980 grazed Japan 1470 12.5 1400 cut, fertilized Japan 1470 12.5 2800 ley Sweden 520 5.4 6.3 5500 Lagerlöfetal, 1989 meadow Poland 533 8.0 6.1-6.5 17000 Ryl, 1977 ryegrass-clover sward New Zealand 971 5.7-6.2 13800 McColl, 1984

Moor

fen Canada 580 2.5 6.4 5600 Dash& Cragg , 1972a Juncus peat England 780 5.6 4.4-4.7 145000 Peachey, 1963 Nardus England 780 5.6 4.8-5.0 71000 blanket bog England 780 5.6 4.4-5.0 40000 Standen, 1973 Carex nigra mire Norway 850 -1.4 22000 Klungland, 1981 Table 2.1,continued

Biotope Country Precipitation Air temperature pH Abundance Author (mm/year) (Ann. mean, 'C) Number/m2)

Forest deciduous, moist Finland 596 3.8 5.1 5700 Kairesato, 1978 deciduous,dr y Finland 596 3.8 5.4 8000 deciduous Canada 580 2.5 6.4-6.7 10000 Dash & Cragg, 1972a deciduous Japan 2000 7.0 22000 Kitazawa, 1971 deciduous, beech Germany (FRG) 1045 6.6 3.3-4.0 108000 Ellenberge t al., 1986 deciduous, beech Germany (FRG) 1017 8.3 3.8-4.7 46000 Römbke, 1988 deciduous, beech Germany (FRG) 613 8.7 5.4-6.4 12000 Meilin, 1988 deciduous, beech Germany (FRG) 700 7.0 6.8-4.3 22300 Schaefer, 1990 deciduous, oak Hungary 627 11.1 18000 Dózsa-Farkas, 1973b deciduous, oak-hornbeam Hungary 643 9.9 22000 Dózsa-Farkas, 1978c deciduous, oak-hazel Sweden 570 5.5 5.0-7.0 3800 Axelssonetal.,1984 deciduous,ash-alde r Poland 5.5 29500 Makulec, 1983 deciduous, oak-hornbeam Poland 4.0 38600 mixed, pine-oak Poland 4.1 39500 coniferous, pine Poland 3.9 35600 coniferous, pine Germany (FRG) 1045 6.6 3.3-4.5 134000 Ellenberg et al., 1986 coniferous Sweden 600 3.8 4.0-4.6 17000 Lundkvist, 1982 coniferous S. Finland 620 4.3 12300 Nurminen, 1967a; coniferous C. Finland 630 2.4 10400 Huhtaetal, 1967 coniferous Canada 1174 9.0 5.7 5700 Marshall, 1974 coniferous, subalpine Japan 943 4.2 3.4-5.0 138000 Kitazawa, 1977 coniferous, subalpine Japan 2000 4.0 10000 Kitazawa, 1971 subtropical rainforest Japan 2000 15.0 10000 tropical rainforest Malaysia 2000 26.5 4.3-4.8 8900 Chibaetal., 1976; Kira, 1976 Liriodendron forest USA 1265 13.3 6250 Reichle et al., 1975 dry sclerophyll Australia 889 8.2 250 Wood, 1971 wet sclerophyll Australia 1144 6.8 1075

Arable land rye Poland 533 8.0 6.1-6.5 9800 Ryl, 1977 potato Poland 533 8.0 6.1-6.5 13000 lucerne Poland 533 8.0 6.1-6.5 5700 sugar beet Poland 533 8.0 6.1-6.5 9600 sugar beet The Netherlands 725 8.4 7.5 30000 this thesis winter wheat The Netherlands 725 8.4 7.5 12000 wheat Canada 341 3.6 7.5 4650 Willard, 1974a Barley Sweden 520 5.4 6.3 8100 Lagerlöfetal., 1989

Enchytraeidaen oinformatio no nspecie scompositio nan dth edynamic so fth evariou s specieswa srecorded . Asa consequence ,specie srelate ddifferences ,tha tmigh t servea sa nexplanatio nfo rth elarg evariabilit yobserved ,ar eno tknown . Inferences cantherefor eonl yb edraw nfo renchytraeid s asa group . Giventhi ssituation , thedat a suggesttha tonl yextrem evalue so fabioti cparameter sma yinfluenc eth esiz eo fpopu ­ lations,an dtha tan ythreshol dvalue so fthes eparameter swil llargel yb especie sde ­ pendent. Other parametersma yals opla ya nimportan t rolei nth edeterminatio no f enchytraeid population sizes,suc ha sth eamoun tan dqualit yo f primaryproductio n (Abrahamsen,1972 ;MacLea ne tal. , 1977),th eproportio no f itenterin gth esoi lsyste m asdea dorgani cmaterial ,th eabundanc ean dactivit yo fth esoi lmicroflora ,an dth e incidencean dquantitativ e importanceo fcompetition ,prédatio nan dparasitism .

10 10' °8 4 + + + A + o + o + 10' " + tg' 8 o •»£> + o o o + + + * + + + + 103 o

O

, , , • 500 1000 1500 2000 2500

Mean precipitation (mm/yr) E

10' - °$8 a3 4 _Q + + A+ 0+ A + O o E o + o 10' 0 o D 10 t OO 0+ + H (D + * ü + + C 10= o (Ö "ö o c m! =5 -15 3 12 21 30 _Q < Temperature

8.5

pH

Figure2.1: Abundance data (y-axes) ofenchytraeids fromvarious habitat types plotted against meanprecipitation, temperature, andpH. +;grassland; A: moor; 0: forest; 0:arableland

11 2.2.2.Abioti c factors

2.2.2.1. Moisture

Asth eenchytraei depidermi s ispermeabl et owate ran dn oprotectio n mechanisms againstevaporatio nar eknown ,i ti sgenerall yassume dtha tthe yar evulnerabl et o droughtan dtherefor econfine dt omois thabitats . Indeed,larg enumber san dbiomas s arefoun di nwe tplaces ,an da numbe ro fspecie sar erestricte dt oaquati co rver ywe t terrestrialhabitats . Healy(1987 )eve nreporte dth efrequen toccurrenc eo fsevera l species ( riparia, Cognettiaglandulosa andCernosvitoviella spp.) inth e deep,anaerobi czon eo fa quakin g marsh. Yet,enchytraeid s alsooccu r indrie rhabi ­ tats,whic hma yb efacilitate db yth efac ttha teve ni ndr ysoil smois tmicrohabitat sma y exist,a sa consequenc e ofth espatia lheterogeneit yo fth esoil . Potwormsma yactivel y movet osuc hplaces ,a sdemonstrate d byvertica lmigratio n indr yperiod s (Peachey, 1963;Das h&Cragg ,1972a ;Springe ne tal. , 1970;Markkula ,1981,1982) . Therear eals oindication stha ta tleas tsom especie sar eadapte dt osurviv ei n drierhabitats ,lik eFridericia galba (Dózsa-Farkas,1977) , Enchytraeusbuchholzi (Trappmann,1952 ;Healy ,1980a) , perpusilla (Klungland,1981) ,Henlea ven- triculosa (Healy,1980a) ,severa lAchaeta species (Healy,1980b )an dth e"Ic eworm" , Mesenchytraeussolifugus (Goodman& Parrish ,1971) . Abrahamsen(1971 )showe d thatCognettia sphagnetorum wasabl et osurviv ei nrathe rari dcondition s (waterpoten ­ tialslightl ybeneat h- 1MPa) ,provide dtha tth etemperatur ewa sno tabov e12°C . Dózsa-Farkas (1977)obtaine dcomparabl e resultswit hFridericia galba. Willard (1974a,b)reporte d rather highnumber so fenchytraeid sfro mprairi esoil si n Canada, wherepotworm s representedon eo fth emajo rgroup so finvertebrates . Asthi sare a wascharacterize d byver ydr ysummer san dsever ewinters ,thes epopulation smus t havebee nver ywel ladapte dt oari dconditions . Thefairl yhig hdensitie san dnumbe ro f speciesHeal y(1980b )foun ddurin ga drough tperio di nFranc ean dSpain ,an dth ehig h numbersreporte db yYeate s (1967,1968)fro mNe wZealan ddun ehabitat sals osug ­ gestth eexistenc eo fadaptation s todr yconditions . Ina ninvestigatio n ofenchytraei dpopulatio ndynamic s intw otype so fScot spin e stands,Gröngröf t &Miehlic h(1983 )foun da significan t positivecorrelatio n between populationdensitie san dth ewate rpotentia li nth emoiste rtyp eo fpin estand ,wherea s inth edrye rstan dpopulation s increasedwhil eth ewate rpotentia ldecrease dt o -0.8 MPa. Inbot htype sth esam especies , sphagnetorum, dominated,sug ­ gestingintraspecifi c physiologicaladaptations . Thus,i twoul dsee mtha tinfluence so fmoistur econdition so nenchytraei dpopula ­ tionsize sdepen do nsevera lfactors ,notabl yspecie scompositio nan dtemperatur e conditions. Enchytraeids mayb eabl et otolerat eextreme s inmoistur econdition sb y

12 physiologicalo rbehaviora ladaptation s atth especie slevel ,o reve nintraspeci fic adap ­ tations. Besides,factor slik esoi lorgani cmatte rconten tan dsoi lstructur ewil lundoubt ­ edlyb eo f importance,a sthes ema ydetermin eth eoccurrenc eo ffavourabl emicrohabi ­ tatsi notherwis e unfavourableconditions . Predictionso fth einfluenc eo fchange si n soilmoistur eo nth edevelopmen to fenchytraei d populations musttherefor etak ethes e factorsi naccount ,an dthei r interactionscertainl ydeserv efurthe rstudy .

2.2.2.2. Temperature

Asca nb einferre dfro mTabl e2.1 , Enchytraeidae arefoun da ta wid erang eo f meanannua lai rtemperatures . Forsom especies ,notabl yfro mth egener a Enchytraeusan dLumbricillus, whichca nb eculture deasil yan dsom eo fwhic har e beingculture dcommercially ,optimu mtemperature sfo rreproductio n havebee nfoun d rangingfro m8° Ct o28° C(Trappmann ,1952 ;Ivleva ,1969 ;Learner , 1972;thi sthesis) . Therang eo ftemperature sa twhic hreproductio n ispossibl e isstil lmuc hwider . Trappmann (1952)reporte da lowe rlimi to f0.5° Can da nuppe rlimi to f 37"Cfo r Enchytraeusbuchholzi an dIvlev a(1969 )mentione da slimit sfo rgoo dreproductiv e success in£ albidus 8an d25°C ,respectively . Thereexis tappreciabl edifference s inth ereactio no fdifferen tenchytraei dspecie s totemperatur e regimes. Klungland (1981)reporte da shar preductio ni nnumber so f Henleaperpusilla withdecreasin gtemperatures ,whil enumber so fBryodrilus ehlersi remained unaffected. Healy(1980b )foun da hig hproportio no fsexuall ymatur eindi ­ viduals inFranc ean dSpai ndurin ga dr yan dwar m (temperatures upt o38°C )period . Dózsa-Farkas(1973a )wa sabl et oprov eexperimentall ytha tStercutus niveus wa sabl e tosurviv eperiod so ffrost ,whil eFridericia-speaes wereno tan dha dt oretrea tt o deeper soillayer st osurvive . Somespecie sar eadapte dt over ylo wtemperatures ,lik e thesubarcti cHenlea cf. udei(Smit he tal. , 1990)an dth eAlaska n"Ic eworm" , Mesenchytraeussolifugus (Goodman& Parrish ,1971) ,whic hlive si nth esno wcove ro f glaciers. Thenatur eo fsuc hadaptation s remainst ob einvestigated ,bu tma yb eo fa biochemical,rathe rtha na structural,origi n(Goodma n& Parrish ,1971) . Itwoul dseem ,therefore ,tha ttemperatur eregime shardl ywoul db ea limitin g factorfo renchytraei dpopulation st oge testablished . Generally,temperatur e mayb e regardeda sinfluencin gspecie scompositio nan dpopulatio ndensity , rathertha n pres­ enceo rabsenc eo fpotworms .

13 2.2.2.3.p H

Largestnumber so f potwormshav egenerall ybee nfoun di nneutra lt oaci d (pH±4 ) habitats. Butals oi nmor ealkalin e (top Habov e8 )habitat slarg epopulation s mayb e found,a sappear sfro mth edat ao fYeate s (1967;1968 )o nth eenchytraei dfaun a of dunegrassland si nNe wZealan dan do f Healy(1980a) ,i na nextensiv esurve yo fIris h enchytraeids. Thespecie swhich ,i nrecen tyears ,wa smos tintensivel ystudie dwit hrespec tt oit s responset ochange si np Hi sCognettia sphagnetorum. This isth edominatin gspecie s innorther nan dtemperat econiferou sforest san dmoors ,an dth erathe rextensiv e literatureo nthi ssubjec toriginate sfro mth e'aci drain 'issu ean dquestion sconcernin g fertilization offorests . Insevera lexperiment sth ep Ho ffores tplot swa smanipulate db y acidification,limin go rfertilizatio n (Lohmetal. , 1977;Abrahamse n& Thompson ,1979 ; Bààthe tal. ,1980a,b ;Huht ae tal. , 1983;Persso ne tal. , 1987). Thegenera ltren di n thesestudie swa stha tC. sphagnetorum reactedpositivel yt osligh tacidification ,afte ra temporary reductioni npopulatio nsize ,an dnegativel yt oliming . Reactiono flumbri - cids,i nthi scas eDendrobaena octaedra, wasth ereverse . Thesefinding swer ecor ­ roborated inmor econtrolle dexperiment sb yHâgva r& Abrahamse n (1980)o n coloni­ zationo fsteril esoi lsample swit hadjuste d pHvalues . However,othe renchytraei d speciesi nthei rexperiment s showedn oconclusiv eo rth eopposit ereaction . Heungens (1984)conducte da shor tter mexperimen twit hC. sphagnetorum and concludedtha tth eeffec to fchange si np H wasinsignifican tcompare dwit hth eeffec to f changes inth eelectrica lconductivit y ofth esoi lsolution . Thisma ywel lb ea n alterna­ tiveexplanatio nfo rth eshock-effec t observedi nvariou sfiel dexperiment so np H ma­ nipulationan dfertilize rapplication . Standen(1980b )reporte da positiv ecorrelatio nbetwee np Han dnumber so fsom e specieso fth egenu sFridericia andC. glandulosa. Ina nothe rstud yStande n(1984 ) founda negativ ecorrelatio n betweenabundanc eo fpotworm san dsoi lpH ,whic hwa s largelyaccounte dfo r byC. sphagnetorum andt oa lesse rexten tb yAchaeta affinis,A. eisenian dC. glandulosa. Otherspecie sshowe dn onegativ eo reve na slightl ypositiv e response,an ddiversit yo fth eenchytraei dcommunitie swa spositivel y relatedwit hsoi l pH. Yeates (1968)foun dlarg epopulation so fHemifridericia sp.an dAchaeta sp.i n neutralt oalkalin e (pH7. 5t o8.6 ) soil. Healy& Bolge r(1984 ) mentioned pHa son e of themos timportan tenvironmenta lfactor sfo rth edistributio n ofenchytraei dspecie si n Irishwetlands . Morespecie sappeare dt ob eaci dintoleran ttha naci dtoleran ti nthes e habitats. Thus,i tma yb econclude dtha tsom eenchytraei dspecies ,notabl yC. sphagne­ torum, clearlyar eacidophili c oraci dtoleran t and,possibl ybecaus eo fth eabsenc eo f competitors,ma yconstitut eth edominan tmesofaun agrou pi naci dhabitats . The ma­ jorityo fenchytraei dspecies ,however ,prefe rslightl yaci dt oalkalin ehabitats .

14 2.2.3. Biotic factors

2.2.3.1. Food and feeding

Datao nth efeedin g mechanismso fterrestria lenchytraeid s arescarce . Adetaile d accounto nth elittora lspecie sLumbricillus lineatus, however,wa spresente db yGelde r (1984). Thisspecie singeste dminera lparticle san dorgani cdebri swit hdiameter sles s than6 0jum ,a nuppe rlimi twhic hwa sprobabl ydetermine db yth emaximu mmout h aperture. Smallparticle scoul db esucke d updirectly ,bu tmostl yingestio ntoo kplac e protractingth epharyngea lpad , thesurfac eo fwhic hwa scovere dwit hadhesiv esecre ­ tionsfro mth epharyngea lglands . Inthi sway ,th efoo dmas sentere dth epharyn xan d wastransporte dt oth eintestin eb yperistalti c movementsan dciliar yaction . Intrul y terrestrialenchytraeid s suchobservation s areno tknown ,bu tavailabl edat a(Hrabë , 1934;Matschek ,1972 )sugges ta simila rfunctio no fth epharyngea lpa di nth eingestio n offood . Head(1967 )observe denchytraeid san dnematode sfeedin go ndecayin groo t cortex,thereb yopenin gchannel stha tallowe dmite san dcollembol at oenter . Toasses sth eimpac to fenchytraei dfeedin go nth efunctionin go fth edecompose r system,knowledg eo nth edie tan dfeedin g preferenceso fenchytraei d species is re­ quired. Animportan tquestio n inthi srespec t is, wetherenchytraeid s shouldb e classi­ fieda sprimar yo ra ssecondar ydecomposers ,i.e .wethe rthe yar esaprovore so r microbivores. Oneapproac ht othi sproble mwa sfollowe db yGotthol de tal . (1967)an dGotthol d &Koc h(1974) ,wh oinvestigate dth enutritiona lrequirement s ofEnchytraeus fragmen- tosus usingaxeni cculture sestablishe dearlie r (Dougherty& Solberg , 1960;1961) . Fromth efac ttha tE. fragmentosus canb eculture di nth eabsenc eo feithe rbacteri ao r fungi,i tma yb econclude d thatthi sspecie si sno ta nobligator ymicrobivor ean dma yb e capableo fobtainin gfoo dfro msource slik edea dorgani cmateria lan droo texudates . Also,Palk a& Spau l(1970 )foun di na nothe rspecies , rivalis (accordingt o Learner, 1972)th ecapabilit y ofdigestin gcarbohydrates ,fat san dproteins . Tob eabl et odecompos edea dorgani cmaterial ,however , itwoul db enecessar y forenchytraeid st oproduc eth erigh tenzymes . Someinformatio n onthi s isfoun di n Nielsen(1962 )an dDas he tal . (1981),wh ostudie denzyme si nvariou sspecie so f enchytraeidsfro m European dIndia ,respectively . Frombot hstudie s itappeare dtha t thespecie sstudie dwer ecapabl eo f digestingdi -an dsom epolysaccharides , buttha t mostcomple x plantsubstance swoul dbecom eavailabl ethroug h microbialaction . Fromfeedin gexperiment swit hCognettia sphagnetorum innorma lan daxeni ccultures , Latter(1977 )an dLatte r& Howso n (1978)arrive da ta simila r conclusion,i.e .tha tthi s species utilizedsimpl eorgani ccompounds ,possibl ythroug hth eactio no fenzyme s and/or microorganisms. Theyfoun dn oindication s ofutilizatio no f microorganisms

15 proper,bu tthi scoul dno tb eexclude deither . Brockmeyere tal . (1990),usin glabele d methionine,demonstrate dtha tEnchytraeus cf. globuliferus andE. minutus digested microorganisms,an dtha tfres hplan tmateria lwa sassimilate ddistinctl y less. Oatbra n however (richi ncarbohydrates ,wit hdeficien tcel lwalls )wa stake n upt oa greate r extenttha nmicroorganisms . Pokarzhevskye tal .(1989 )pointe dout ,tha ti nvie wo fth eamount san dform so f nitrogen andphosphoru srequire dt omaintai nsoi lanima lpopulations ,microorganism s mustpla ya nimportan tpar ta sa foo dsource . Again,base do nß 13C measuremento f earthwormtissue ,plan tmateria lan dsoil ,Spai ne tal . (1990)argue dtha tth eglos - soscolecidearthwor mPontoscolex corethrurus derive dmuc ho fit stissu ecarbo nfro m rhizosphereproduct san dmicrobia lbiomass . Consumptionan ddigestio no ffung ib y severalenchytraei dspecie swa sreporte db yDas h& Crag g(1972b )an dDas he tal . (1980),s otha tassimilatio no fa tleas tpar to fth ecel lcontent so fth efung iwoul dsee m area lpossibility . Inth egu tcontent so f2 ou to f3 investigate dspecies ,O'Conno r (1967)foun dsignificantl y morefunga lmateria ltha ni nth esubstrate . Dash& Crag g (1972b)als oreporte do nhig hproportion so ffung ii nth egu tcontent so f4 specie s investigated,an dselectiv efeedin go nfunga lbait si na fiel dexperiment . Ina nultrastructura lstud yo fth egu tcontent so fFridericia striata, Toutaine tal . (1982)foun dtha tingeste d plantmateria l underwent littlechang edurin gpassag e throughth egut ,whil eassociate dbacteri aan dfung iwer elyse dsoo nafte ringestion . Gelder (1984)als opresume dth eutilizatio no forgani ccompound san dbacteri ab y Lumbricillus lineatus. Dózsa-Farkas(1976 ;1978a )studie dth econsumptio n oflea f litter by galba,F. hegemon andHenlea nasuta. Itappeare dtha tleave sha dt ob edecomposin g tob econsumed ,th epreferenc efo rdegre eo fdecompositio n andtre especie s beingno t onlydependen to nspecies ,bu tals oo n theseason . Fortubifici dworms ,digestio no f (Gramnegative ) bacteriaha sals obee nsuppose dt ob equantitativel y important (Whitley& Seng ,1976) . Zachariae (1963)reporte do nenchytraeid s consumingcollembola nexcrements , andPong e(1984 )found ,beside splan tremain san dmicroorganisms ,excrement so f oribatidmite si nth egu tcontent san dsuggeste da relatio nwit hfung igrowin go nthes e excrements. Breakdowno f plantmateria ldurin gth epassag ethroug hth egu tha sno t beenobserve di nth estudie smentione dabove . Variousauthor smad ea microscopica lstud yo fth egu tcontent so fenchytraeids . Insevera lo fthes estudie sconsiderabl eamount so fsilic aparticle swer ereporte d (O'Connor, 1967;Babel ,1968 ;Matschek , 1972;Gelder , 1984;thi sthesis) . Fromhisto - physiological observations onLumbricillus lineatus byGelde r (1984)i tseem sprobabl e thatsuc hparticle sar ebein gtake nfo rth emicroorganism san dorgani cmaterial so n theirsurface . Theabov ementione d resultspoin tt oth eimportan tpar tplaye db ymicroorganism s andthei ractivitie s inth efeedin gbiolog yo fenchytraeids . Obviously,enchytraeid sar e

16 alsocapabl et outiliz eeasil ydigestibl eorgani ccompound stha tar eproduce db yplants , orthroug hth eactivit yo fmicroorganisms ,bu tcompetitio nwit hth emicroflor amigh tb e limiting inthi srespect . Asonl ya restricte d numbero fspecie s havebee ninvestigate d sofar ,specie srelate ddifference s infeedin gactivitie sremai nt ob e investigated. Inproductio necologica lstudie senchytraeid s areofte nconsidere d asbein g 50% saprovorous,25 %bacterivorou s and25 %fungivorou s (Perssone tal. , 1980;Lagerlö f et al., 1989). Theavailabl eevidenc esuggest stha ti nthi swa ymicrobivor yma yb eunder ­ estimated,sinc ea tleas tsom especie so fEnchytraeida ear ewel ladapte dt odiges t microbes,whil en ospecie shav ebee nfoun dtha tproduc eenzyme sneede dt o decom­ posecomple xvegetabl ecompounds . Theassumptio no fWhitfiel d(1977 )an d MacLean (1980),tha tenchytraeid sar e80 %microbivorou san d20 %saprovorous ,ma y bemor erealistic .

2.2.3.2. Competition

Littlei sknow nabou tcompetitiv einteraction s between Enchytraeidae andothe r soilorganisms . Healy(1980a )believe dtha tth eabundanc eo fenchytraeid s isrelate d tocompetition ,notabl ywit hearthworms ,fo rfood ,an dtha thig hdensitie so fpotworm s arefoun di ncase swher ealmos tn ocompetitio n occurs,a si nextremel y acidenviron ­ ments. Somespecies ,lik eCognettia sphagnetorum, arever ywel ladapte dt osuc h environments,an dreac hhig hdensitie sthere . Competitionfo rfoo dma yals ooccu r betweenenchytraeid s andmicroarthropods ,a ssuggeste d byWa y& Scope s(1968) , whofoun da significan t increase inenchytraei d numbersafte rapplicatio no finsecti ­ cidesan dth eresultin gsever ereductio no f microarthropodnumbers . From experi­ mentsb yAlejnikov ae tal . (1975)an dLagerlö f &Andre n(1985) ,wit hdecomposin g manurean dbarle ystraw ,respectively , itappear stha tpotworm smainl yparticipat ei n theearl yphase so fdecomposition ,an dar efollowe d bymicroarthropods . Towha t extentcompetitio n playsa rol ei nthi sproces s isunclea ra sthes eresult s mayals o indicatedifference s infoo dpreferenc ebetwee nbot hgroups . Severalauthor s havesuggeste da nantagonisti crelationshi pbetwee n enchytraeids andearthworms . Nielsen(1955c )believe dth eecologica lstatu so fbot h groupst ob ecompletel ydifferent ,an dthei rabundance st ob enegativel ycorrelated . Thisvie w ispartl ycorroborate db yGóm y(1984) ,wh oi nDutc hpolde rsoi lfoun dles s potwormsi nplot sinoculate dwit hearthworms ,a soppose dt ocontro lplots . The an­ tagonisticeffec tseeme dt ob einterspecifi chowever ,rathe rtha nt oexis tbetwee nth e twogroups . Theautho rsuppose dtha tsecretion so rexcrement s mightpla ya par ti n thisprocess . Ina breedin g experimentwit hEisenia fetida andEnchytraeus albidus, Haukka (1987)observe dimpede dgrowt ho fE. fetida athig htemperatures ,bu tfaste r growtha t lowertemperature swhe nE. albiduswa spresent . Moreover,i nth epresenc eo f

17 E.albidus mortalityo fE. fetida increased. Asbot hspecie sshowe doptima lpopulatio n developmenta tdifferen t moisturelevels ,i tappeare dlikely ,however ,tha t innatura l situationsthe yoccup ysomewha tdifferen tniches . Positiverelation sbetwee nearthworm san denchytraeid shav eals obee n ob­ served. Zachariae(1967) ,fo r instance,mentione dtha tpotworm sconsume dth eexcre ­ mentso flumbricids ,thereb ypromotin gdecompositio no fenclose dlitter ,tha tcoul db e consumedonc emor eb yearthworms . Bhatti(1967 )reporte dassociation so f enchytraeidswit hth eearthworm sBimastos parvus andPheretima posthuma, andwit h Collembola. Dózsa-Farkas (1978c)foun dsignificantl y moreenchytraeids ,notabl y Fridericia galba andStercutus niveus, inearthwor mburrow stha twer efille dwit hlitter . Theautho rassume dtha tth elitte r inthes eburrow swa sattractiv efo rth eenchytraeid s becauseit sstat eo fdecompositio nwa sfavourable . Itma yb econclude dtherefore ,tha tsom especie so f Enchytraeidae mayhav eth e samerequirement sa searthworms ,bu tar ebette radapte dt oextrem e (notablyacid ) situations,an dar eno tabl et ocompet ewit hearthworm s inothe rsituations . Themajor ­ ityo fenchytraei dspecies ,however ,hav emor ecomple xrelation swit hearthworms ,an d thusoccup ya tleas tpartl ydifferen t niches. Thusfar ,n oconclusiv eevidenc eha sbee n presentedfo rcompetitio nbetwee nenchytraei dspecie san dothe rmember so fth esoi l fauna.

2.2.3.3. Predators and parasites

Thenumerou soccurrenc eo f Enchytraeidaean dth eapparen tlac ko f protective mechanismsmak ethe ma nobviou spre yfo r predatorysoi lanimals . Yet,fe wstudie s mentionpredator so fenchytraeids ,an dn oquantitativ edat ao nth esubjec texist . Ina reviewo npredator ysoi lnematodes ,Smal l(1987 )liste da numbe ro ftaxa ,notabl y larger Dorylaimidaan dMononchida ,tha twer efoun dt ofee do npotworms . Formos to f thespecie s listed,however , iti sno tclea rwhethe rliv eo rdea denchytraeid swer e consumed. Directobservation so f prédationo nenchytraeid swer ereporte donl yi nth e speciesAnatonchus amicae (Coomans& Lima ,1965) ,Prionchulus punctatus (Small, 1987),Nygolaimus vulgaris (Thome,1930) ,Sectonema ventralis (Thome,1930 )an d Butlerlus degrissei (Grootaerte tal. , 1977). Yeates (1968)demonstrate da positiv e correlation betweenth eabundanc eo fsevera lpredator ynematode san denchytraeids . Sergeeva(1987 )analyze dth egu tconten to fsevera lpredator ysoi linvertebrate s withserologica lmethods . Itwa sfoun dtha tth elarva eo fth erhagioni dflie s Ragio scolopaceus andR. tringarius, especiallyth esmalle rones ,probabl yfe dt oa larg e extento nenchytraeids . Inth egu tcontent so fsmal lan dmedium-size dindividual so f thecentiped eMonotarsobius curtipes andlarva eo fth eelateri dbeetl eDolopius margi- natusals oenchytraei dmateria lwa sestablished . Theadult so f severalspecie so f carabidbeetles ,notabl yAbaxater an dA. parallels, werereporte db yLorea u (1983)t o

18 preyo noligochaete s (enchytraeidsan dlumbricids )t oa considerabl eextent . Nielsen (1955b),probabl yo nth eauthorit yo f Kühnelt (1950),mention sprédatio nb yth e centipedeSchendyla nemorensis, butconsider s itsimpac tmarginal . Somemesostig - matidmite sma ypre yo npotworms ,a sSinge r& Kran z(1967 )successfull y used enchytraeids asa foo dsourc ei nculture so fth egamasi dmite sMacrocheles superbus, M. robustulus andGlyptholaspis confusa, andHeungen s (1969)suggeste dtha tth e gamasid miteParholaspulus alstoni migh tb ea ninfluentia lpredato r onenchytraeid si n Azaleacultures . Parasiticorganism sassociate dwit hpotworm shav ebee nrecorde dfro mvariou s taxa,o fwhic h Protozoasee mt ob eth emos tfrequentl y occurring. Gelder (1984)re ­ portedth eoccurrenc eo fSporozo ai nth ealimentar ycana lo fLumbricillus lineatus. Accordingt oPurrin i(1983,1987) ,enchytraeid s arefrequentl yinfecte d bymicroorgan ­ isms,especiall y inpollute dareas ,wher einfectio nrate sma yb ea shig ha s 70%. Pathogenicagent sidentifie dwer evirus-lik eorganisms ,Bacteria ,Fung ian dProtozoa . Infectioncoul doccu r invariou stissues ,an dfrequentl y causedletha ldiseases . Among theorganism s identified,gregarini d Protozoawer eth emos tabundant ;thes eorganism s wereprobabl yno tparasitic ,however ,an dlive da scommensal s inth egu tlumen . Nielsen(1955b )als oreporte dth eincidenc eo f Gregarinidai nenchytraeids ,an dnote d thatth einfectio n ratewa sa tit smaximu mi nth esumme rhal f ofth eyear . Ciliatesar e reportedt ooccu rcommonl yi nth egu to foligochaete s (Hartwig& Jelinek ,1974 ; Righi, 1974). Kunst(1954 )reporte d onsevera lparasiti c Rotatoriafro mth egenu s Balatro, livingi nth egu to fpotworms . Taboga(1981 )reporte dfacultativ e parasitismo n earthwormcocoon sb yth esaprophyti c nematodeRhabditis terricola. Althoug ha sye t notreported ,i twoul dsee monl ynatura ltha t productivity lossesthroug hsuc hmecha ­ nismsals ooccu ri nth eEnchytraeidae . Noquantitativ edat aexis to nth eimpac to fprédatio nan dparasitis mo nenchytraei d populations. Yet,i nvie wo fth equalitativ eevidence ,an dnotabl yth evariet yo fpreda ­ torsan dparasite s reported,i tseem sobviou stha tsubstantia llosse sthroug hthes e interactions mayoccur . Thus,i tma yb eworthwhil et ostud ythes eprocesses ,tha t mightinfluenc eenchytraei d populationdynamic st oa considerabl edegree .

19 2.2.4. Man induced factors

2.2.4.1. Physical habitat changes

Physicalhabita tchange sclearl yma yinfluenc eenchytraei dcommunities ,whic h specifically mayb edemonstrate d inarabl esoils . Importantfactor stha tpla ya par ti n thisrespec tar eeffect s ofchange si nsoi lstructure ,th ereductio ni nth eamoun to f primaryproductio n reachingth esoi la sdea dorgani cmaterial ,an dth ereduce ddiver ­ sityo f plantspecies . King& Hutchinso n (1976,1983)an dHutchinso n& Kin g(1980 )studie dth eeffect s ofshee pstockin g intensityo ninvertebrat e communities inAustralia npastures . Enchytraeid numbers,biomas san dactivit ywer einversel y relatedwit hth egrazin g pressure. Theeffect s couldmainl yb eattribute dt oa reductio ni nhabitabl epor espace , changesi nmicroclimatologica lregime san da reductio n infoo dsupply . Brockmanne t al. (1980)als oreporte da significan t reductiono fenchytraei ddensitie s ina fiel dexperi ­ mentwit hsoi lcompaction . Acomparabl eeffec to f soilcompactio nwa sfoun db y Dózsa-Farkas (1987a),wh ofoun da significan t decreasei nenchytraei d densitiesan d diversityi nHungaria nhikin gtrails . Onespecies ,Fridericia conculcata, however, seemedadapte dt othes ecompacte dsoils ,an deve nshowe dhighe rincidenc ethere . Effectso fsoi ltillag eappea r clearestwhe nth eto psoi li sinverted . Severalinvesti ­ gators (Zimmermann,1987 ;Lagerlö f etal. , 1989;thi sthesis ) haverecorde da mor e evenvertica ldistributio no f Enchytraeidae inploughe dplots ,o reve na concentratio ni n thedeepe r layers,wher eafte rploughin gth eplan tremain sar et ob efound . Moreover, Tomlin& Mille r (1987) recordedstil la neve nvertica ldistributio no fsoi lfaun a(includin g enchytraeids) ina formerl y ploughedplo ta tleas t2 5year safte rcultivatio nstopped . Whilemuc hinformatio n existso nth edetrimenta leffect s onearthworm s ofmos ttype s oftillage ,n oindication shav ebee nfoun dfo rsuc heffect so npotworms . Probably,thi s hast od owit hth esmalle rsiz eo fenchytraeids ,renderin gthe mles svulnerabl et oth e tillageaction ,wit hrelativel yles sdisturbanc eo fthei r microhabitats,an dwit hthei rfaste r modeo freproduction . Lesscompetitio nwit hth ediminishe dearthwor mpopulation s may,however ,als opla ya part .

20 2.2.4.2. Chemicals

Inassessin gth eimpac to fth eapplicatio no f chemicalsubstance s (pesticides, fertilizers,pollution ) onenchytraei dcommunities ,i ti simportan tt odiscriminat e between short-terman dlong-ter meffects . Short-termeffect s concerndirec teffect sthroug h toxicityo fth esubstance sapplie do rchange s inth ephysica lan dchemica lpropertie so f theenvironment ,an dar efoun da slon ga sth eforeig nsubstance sar epresent . Long- termeffect s aremanifeste dthroug h moreo rles spermanen tchange s infoo dsupply , changes incompositio no fth esoi lcommunit yo rth ephysica lenvironment ,o rgenetica l adaptationwithi npopulations .

2.2.4.2.1. Pesticides

Directtoxi ceffect s ofth eherbicid e2,4,5- T(2,4,5-Trichlorophenox yaceti cacid )o n severalenchytraei dspecie shav ebee nobserve d inlaborator y experiments byRömbk e (1988). Itappeared ,tha tth eeffec twa sspecie sdependent , albidus being lesssensitiv etha nC. sphagnetorum, Marionina cambrensis andAchaeta cf. affinis. Besides,kin dan dacidit yo fth esubstrat ewer eimportant ,th eeffec t beinggreate ri n moreaci dsubstrates . In fieldexperiment si na beec hforest ,wher e2,4,5- Twa sbi ­ monthlyapplie dfo ra perio do ftw oyears ,thes eresult swer eonl ypartl ycorroborate d (Römbke,1988) :C. sphagnetorum appearedt ob ehardl yinfluence d here. Enchytraeid abundancean dbiomas swer ealmos tunaffecte da tlow ,bu treduce da thig hdosages . Afterth eapplicatio n hadstopped ,enchytraei d numberstemporaril ywer ever yhigh , returningt oth econtro lleve lafte rtw oyears . Chalupsky (1987,1989)reporte da simila r effect aftera singl eapplicatio no fatrazin ei na norchard ,enchytraei d numbersbein g slightly loweredth efirs tyea rafte rth eapplicatio nan dhighe rth esecon dyear . In the sameexperimen t continuous applicationo f herbicidesreduce denchytraei ddensitie s significantly. Theresult sobtaine db yBäumle re tal . (1978),wit h Paraquatan d Simazin infores tsites ,poin ti nth esam e direction. Andren& Lagerlö f (1983)als oreporte da negativ eeffec to nenchytraei dpopula ­ tionso fyearl yapplication so f MCPA,Dinoseb ,2,4,5- Tan d2,4-Dichlorophenox yaceti c acid(2,4-D ) inpasture ,bu tdi dno tfin da neffec t inarabl efields . Again, Weber(1953 ) coulddetec tn oeffec to fa singl eapplicatio no f2,4- Di narabl efields . Fromth eavailabl edat ai twoul dsee mtha t asingl eapplicatio no fa herbicid ema y resulti ninitiall ylowe renchytraei d numbers,probabl ythroug ha direc t effect,an dfol ­ lowedb ytemporaril y unusually highnumbers ,presumabl ythroug hextr aavailabilit yo f deadplan tmaterial . Theseeffect swer eals ofoun di nothe r soilfaun agroup slik e nematodes,mite san dcollembol a(Bäumle r etal. , 1978;Andre n& Lagerlöf ,1983) .

21 Continuousapplicatio no f herbicideswil llea dt oa permanen tdecreas eo fenchytraei d densitiesan ddiversity ,a sa resul to fth ereductio ni nwee dproductio n andplan tspe ­ ciesdiversity .

Fewstudie saddres sth eeffec to ffungicide so npotworms . Bethke-Beilfuß &West ­ heide(1987 )demonstrate di nlaborator yexperiment ssubletha ldamage ,notabl yre ­ ducedfertilit y andhatchin g success,cause db yBenomy li ntw o Enchytraeus-spec\es, althoughbot hspecie sdiffere d markedlyi nthei rsensitivit yt othi sfungicide . Römbke (1988,1989b)foun dconsiderabl e mortality inE. albidus atlo wdosage so f Benomyl andPC P(Pentachlorophenol ) inlaborator yexperiments ,an deve nhighe rsensitivit yt o PCPwit hC .sphagnetorum, M. cambrensis andA. cf. affinis. In fieldexperiment swit hregula rapplicatio no f Benomyl (Niklas,1980 ;Andre n & Lagerlöf,1983 )suc heffect s haveno tbee nobserved . Niklas(1980 )eve nobserve da slightincreas e inenchytraei d numbersi nBenomy ltreate d plots,whic hsupposedl ywa s connectedwit ha reductio n inlumbrici dnumbers . Fieldexperiment swit hbimonthl yapplicatio no f PCPi na beec hfores t (Römbke,1988) ,showe dtha tthi sfungicid ereduce denchytraei dabundanc ean dbio - masssignificantly ,an dtha tth epopulation s recoveredonl yslowl yafte rth eapplicatio n hadstopped . Notal lspecies ,however ,reacte di nth esam eway :C. sphagnetorum, Mesenchytraeusglandulosus, andAchaeta sp. wereclearl ynegativel yinfluenced , whileothers ,lik eMarionina clavata, M. cambrensis, andC .cognettii appeare dt ob e almostinsensitiv et othi sfungicid eunde rfiel dconditions . Again,th efungicide sTP N (Chlorothalonil),i nafiel d experiment (Kitazawa& Kitazawa,1980) ,an dTrichlorotrinitrobenzen e (TCTNB),i na po texperimen t (Heungens,1970) ,prove dt o reduceenchytraei dnumber sconsiderably . Invie wo fth eprobabl efoo drelatio nbetwee nfung ian dpotworm sdiscusse d above,a negativ eindirec teffec t offungicide so nenchytraei ddensitie si nth efiel dmigh t beexpected . Assuc heffec tcoul dno tb edemonstrate d inal lcases ,thi sma yindicat e littlefoo dselectivit y inth especie sconcerned ,o ra shif ti nspecie scompositio ntoward s lessselectiv especies .

Someinsecticide s andnematicide s(Parathion ,Carbofura nan dTerbufos ) havea short-termtoxi ceffec to npotworm sunde rlaborator ycondition s(Bethke-Beilfu ß &West ­ heide,1987 ;Hagen s& Westheide ,1987 ;Römbke ,1989b) . However,o fNemagon , Aldrinan dLindan e (hexachlorcyclohexane, BHC)n oclea reffect s couldb edetecte d (Radue tal. , 1970). Asth etes tprocedure s betweenthes einvestigator svarie dconsid ­ erably,thes eresult s hardlyca nb e compared. Theresult s offiel dobservation s onth eeffect s of insecticides,acaricide san d nematicides oftensee minconclusive . Oforganochlorin ecompound s neutral,positiv e aswel la snegativ einfluence sar ereported . Richter (1953),samplin gfo r oneyea rafte r asingl eapplicatio n ofa norganochlorin e insecticidei npin eforest ,foun dn oeffec to n

22 oligochaetepopulations ,an dneithe r didGrigor'ev a(1953) ,wh osample dthre emonth s afterapplication . Heungens (1969)als oreporte dn oeffec to fa singl eapplicatio no f Aldrinafte r 12weeks ,an dEdward se tal . (1967)detecte dn oeffect s ofAldri nan dDD T duringon eyea ri nagricultura lfields . Theorganochlorin ecompoun d Lindanewa s reported byDormidontov a(1973 )t opromot epopulation so f Enchytraeidaei na po t experimentwit hcompost ,durin gtw oyear safte rtreatment . Kitazawa& Kitazaw a (1980)als oreporte dlarge r populations inagricultura lplot streate dwit hthi sinsecticid e during4 t o6 month safte rapplication . Negativeeffect so f organochlorine compounds onenchytraei d populations,lastin gsevera lweek so rmonth safte rtreatment ,wer e reportedfo r Lindaneb yWebe r (1953),i nagricultura lsoil ,an dHuht ae tal . (1967),i n pinefores t soil;fo r Dicofolb yHeungen s (1970),i na po texperiment ;an dforToxaphen e byBäumle re tal . (1978),i nfores tsoil . Edwards& Arnol d(1966 )state dtha tHexachlo r wastoxi ct oenchytraeid sunde rfiel dconditions . Organophosphorus compoundsar econsidere d byEdward s& Arnol d(1966 )t o havea shor tter mnegativ einfluenc eo nenchytraei dpopulations . Indeed,suc hshor t termeffect swer ereporte dfo r Parathion byWebe r (1953),i nagricultura lfields ,an dfo r Thionazinan dDimethoat eb yHeungen s (1970),i na po texperiment . McColl(1984) ,o n theothe r hand,samplin g monthlyfo ron eyea rafte ra singl eapplication ,detecte dn o effectso fth eorganophosphoru s nematicidePhenamiphos ,an dWa y& Scope s(1968 ) reportedsignificantl y morepotworm ssevera lmonth safte rtreatmen to f agricultural plotswit hth eorganophosphoru s insecticidePhorate . Edwards& Loft y (1971)mentione da significan t reduction inenchytraei d numbers during8 week s afterapplicatio no fth ecarbamat einsecticid ean dnematicid eAldicarb , butn oeffec t ofth enematicid e Methomyl. Heungens(1970) ,samplin g 10week safte r applicationi na po texperiment ,foun dn oeffec to fAldicarb ,an da negativ eeffec to f Propoxur;th esam eautho r (Heungens,1969 )als oreporte dn oeffec to fth ecarbamat e insecticideCarbary l 12week safte rapplication . McColl(1984 )als oreporte d noeffect s ofa singl eapplicatio no fth ecarbamat enematicid eOxamy ldurin gon eyea rafte rappli ­ cation. Didden (chapter3 ,thi sthesis )foun da significan t depressiono fenchytraei dnum ­ bersafte ra singl esoi lfumigatio nwit hth enematicid e D-D (1,3-dichlorodipropene),a n effectwhic hwa sdisappeare dafte rtw omonths ,whe ndensitie sha dreturne dt oth e controlvalue . Thenematicid e Dazometwa sreporte db yEdward s& Loft y (1971)t o causea significan t reductiono fenchytraei dnumber sdurin g8 week safte rapplication . Van DenBrand e& Heungen s (1969),samplin g about1 0month safte rapplication , foundn oeffec t ofa nannua ldisinfectio nwit h D-D,an dHeungen s (1969)reporte d higherenchytraei ddensitie s 12week safte rapplicatio n ofDBCP . Fromth evariet yo fobservation s underfiel dconditions ,i tma yb econcluded , that notonl yth etyp ean dquantit yo fcompoun dused ,an dth ewa yo fapplication ,bu tals o thetim epasse dsinc eth eapplicatio no fa ninsecticid eo rnematicid ear eimportan tfo r establishingthei r effects,an dthat ,moreover ,suc heffect s probablyar eintimatel y

23 relatedwit h propertieso fth eecosyste mstudied . Thegenera limpressio nappears ,tha t bothinsecticide s andnematode s mayproduc eshort-ter mnegativ eeffect so n enchytraeiddensities . Insom ecases ,thei rapplicatio nma yeventuall y resulti nhighe r potwormdensities . AsWa y& Scope s(1968 )suggested , thisma yhav et od owit ha decreasei ncompetitor s orpredators ,kille db yth epesticides . Sincelittl eo rn o re­ searchha sbee nconducte do nth especie s level,however ,i tremain sunclea rwethe r application ofsuc hpesticide s mayresul ti na shif ti nspecie scompositio nand/o rfunc ­ tioningo fth eenchytraei dcommunity .

2.2.4.2.2. Fertilizers

Asenchytraeids ,lik emos tothe rsoi lorganisms ,depen do norgani cmatte ra sa sourceo fenerg yan dnutrients ,i ti sno tsurprisin gtha tgenerall yhighe r abundancesar e reportedfro msite swher eorgani cfertilizers ,lik ecro presidues ,compost ,an dmanures , areapplie d(amon gother s Franz, 1953;Alejnikov ae tal . (1975); Kitazawa& Kitazawa,1980 ; Lagerlöf &Andre n(1985)) . Possiblechange si nspecie scomposition , resultingfro mth eapplicatio no forgani cfertilizers ,hav eno tbee ninvestigated . Effectso fth eapplicatio no f inorganicfertilizer s onenchytraei dcommunitie sma y occurdirectl ythroug hchange si nth eelectrica lconductivit yo fth esoi lsolutio n (Heungens,1980 ;1984 )an dindirectl ythroug hthei rinfluenc eo nprimar yproductio n andth esoi lmicroclimate . Ina numbe ro fstudie sa ninitia lnegativ eshock-effec twa s followedb ya nincreas ei nenchytraei dnumber s (Huhtae tal. , 1967,1969; Marshall,1977 ;Loh me tal. , 1977;Hotanen ,1986 ;Nakamura ,1988) . Abrahamsen & Thompson(1979 )recorde da chang ei nspecie scompositio nfollowin gure afertilizatio n ofa coniferou sforest ,indicatin ga specie sdependen tsensitivity . Marshall(1974 ) reportedsignificantl y lowerdensitie san da mor edownwar ddistributio no f enchytraeids inconiferou sfores tafte ra singl eapplicatio no f urea, theeffec tbein gmos tmarke d betweenth e5 than d8 lhmont hafte r application. Again,i n Polishmeadow stha twer e fertilizedyearl ywit hnitrogen ,potassiu man dphosphorus , Makulec (1976)recorde d lessenchytraeids ,wit ha mor edownwar ddistribution ,tha ni ncontro l plots. Thesedif ­ ferenceswer emainl yattribute dt odifference s insoi lmoistur eregim ea sa resul to fth e applicationo ffertilizers ,bu tther ewer eals oindication so fa shif ti nspecie scomposi ­ tion. Utrobina(1976 )investigate dth einfluenc eo ffertilizatio n ofpotato-field swit h am­ monia-water, andfoun dtha tenchytraei ddensitie ssometime swer eslightl y lessi nth e firstmonth safte rapplication ,whil evertica lmigratio nt odeepe rlayer soccurred . After­ wardsenchytraei dabundance si nth etreate d plotsincrease dabov eth econtro l values. Standen(1984 )showe dtha tenchytraei d biomassi nfertilize dha ymeado wplot swa s negativelycorrelate dwit hphosphoru sfertilization ,bu tdi dno tfin da relatio nwit hor -

24 ganicfertilizatio n ornitrate . Ina nearlie r studyStande n (1982)foun dnegativ ecorrela ­ tions betweenth enumbe ro fenchytraei dspecie san dth eapplie damoun to fnitrat ean d sodium. Asfertilizer s areapplie dt oenhanc eprimar yproduction ,i tmigh tb eexpecte dtha t thesoi lcommunity ,includin genchytraeid swoul dbenefi tfro mthei ruse . Yet,fo rsev ­ eralreason srealit yseem st ob emor ecomplex . Inth efirs tplace ,a ninitia lnegativ e effect,whic hma ylas tfo rsevera lmonths ,ma yoccu rthroug hdirec ttoxi ceffect so r changes inth esoi lmicroclimatologica lregime . Secondly, inmos tcase swher efertiliz ­ ersar eapplied ,th emajorit yo fprimar yproductio n isremove dfro mth esit eo fproduc ­ tion, resulting inles sdea dorgani cmateria lenterin gth esoi lsystem . Thirdly,fertilize r applications inmos tcase sresul ti nles sdivers eplan tcommunitie san dhenc eles s diversedea dorgani cmaterial ,reducin gth enumbe ro fniche sfo rsoi lorganisms . Thus, applicationo f inorganicfertilizer s mayi nsom ecase seventuall y result inhighe rdensi ­ tieso fenchytraeids ,an di nalmos tal lcase si na reduce dspecie sdiversity .

2.2.4.2.3. Pollution

Littleresearc h hasbee ndirecte dt oth eimpac to fpollutant so nth eenchytraei d fauna. Thelittora lspecie sLumbricillus lineatus hasbee nfoun dt ob equit eresistan tt o oilpollutio nan deve nt ob ecapabl et oexcret eoi ldérivâte so rstor ethe mi nit sbod y tissue(Gier e& Hauschildt ,1979) . Thisspecie smigh tb erathe rexceptiona li nthi s respect,a sCoate s& Elli s (1980)foun di tt ob epredominan t inth eoutfal lare ao fa pul p mill,wherea s inles scontaminate darea sth especie swa sreplace db yassociation so f otherenchytraei dspecies . Pirhonen& Huht a(1984 )conducte da fiel dexperimen ti n whichfue loi lan dhydrauli coi lwa ssprea do nfores tsoi lplots . Theenchytraei dpopula ­ tiondisappeare dcompletel yfro mth efue loi lplots ,an dstarte dt obuil du pagai nonl y after 18months ,bu ti nth eplot swit hhydrauli coi lhal fo fth epopulatio nsurvive dth e treatment. Cianciara& Pilarsk a(1983 )reporte do na decreas ei nnumbers ,o reve n completedisappearanc eo fenchytraeid s inPolis hmeadow sexpose dt oai rpollutio n fromactivitie so fcoa lindustry . Heungens (1970)showe dtha tenchytraei dpopulation s mayb esensitiv et otreatmen to fth esoi lwit hcoppe rsulphate . Theinfluenc eo fin ­ creasedconcentration so fcopper ,zin can dlea do nenchytraeid swa sstudie db y Bengtsson& Rundgre n(1982 )an dBengtsso ne tal . (1988),wh ofoun da stron greduc ­ tion, bothi nabundance ,numbe ro fspecie san dactivity . Informe r refusetip si nGer ­ many,Brockman n (1984)foun drapi dcolonizatio nb ypotworms ,whic hindicate sresis ­ tancet oextrem econdition si na tleas tsom e species.

25 Clearly,th eeffect so fxenobioti csubstance so nenchytraei dcommunitie sar e diverse. Duet othei rpermeabl eepidermi sthe yar esensitiv et odirec tcontact ,an d specieso fth egenu sEnchytraeus, thatar erelativel yeas yt oculture ,wer etherefor e proposedb yRömbk e(1989a )an dRömbk e& Knacke r (1989)a stes torganism si n toxicitytests . Onth eothe r hand,a strul ysoi ldwellin gorganisms ,the yar eles slikel yt o comeint odirec tcontac twit hth esubstance sa ssuch ,a slon ga sthes ear eapplie do n topo fth esoil . Thiswoul dimply ,tha tthe ymainl ywil lb econfronte dwit hresidue san d withindirec teffect svi aothe r memberso fth esoi lcommunit yan dth elivin gplants . The highincidenc eo fpathogen san dparasite si nenchytraei dpopulation s inpollute dareas , reportedb yPurrin i(1983,1987) ,i sa nexampl eo fa nindirec teffect ;apparentl yth e vitalityo fth eenchytraeid s isimpaire di nthes eareas . Asmos tenchytraei dspecie s seemt ob eabl et oreproduc equickly ,a singl eexposur et oa harmfu lcompoun d mayb e overcomerapidly . Repeatedexposure ,however ,ma yresul ti nles sdivers ecommuni ­ ties. Importantfactor sdeterminin gth eimpac to fxenobioti c substanceswil ltherefor e be: - Thefrequenc ywit hwhic hsuc hsubstance sente rth esoi l system. - Thepersistenc eo fth ecompoun dan dit sresidues . - Thewa yo fapplication . Sprayingo rdustin gxenobiotic swil linfluenc eenchytraeid s lessreadil ya sdoe ssoi l fumigation. - Thephysiologica leffect so fth exenobiotics ,o rth eabilit yt odea lwit hthem . Earth­ wormsar ereporte dt ob ecapabl eo f biodégradationthroug hhydrolysi so fxenobi ­ oticsubstances ,notabl yorganophosphoru s compounds (Parke tal. , 1990). Itma y beworthwhil et oinvestigat et owha texten tsuc hmechanism s mayb eactiv ei n enchytraeids. - Theimpac to nothe rlivin gorganism stha tar eo f importancefo rth eenchytraeids , asfood ,competitor so rpredators . - Soilcharacteristic s (structure,texture ,organi cmatte rcontent ,moistur econtent ) willt oa larg eexten tdetermin eth eresidenc etim ean dactivit yo f chemical com­ poundsi nsoil .

26 2.3.Th erol eo fEnchytraeida e inecosyste mfunctionin g

2.3.1. Introduction

Theimportanc eo f Enchytraeidae inecosyste mfunctionin gwil l bedetermine db y populationsizes ,specie scompositio nan dtyp ean dleve lo factivity . Speciescomposi ­ tionan dpopulatio nsize sar edetermine d byvariou sfactors ,a sdescribe di nth e previ­ ousparagraphs . Furthermore,th espatia lan dtempora lvariabilit yo f populationswil l causeth eeffect s ofenchytraei dactivit yt osho wa relate dvariability . Importantaspect s ofecosyste mfunctionin gwher einfluence so fenchytraei dactivitie s mayb ereflecte d arenutrien tcyclin g andsoi lstructure .

2.3.2. Soil structure

Amongothers ,Zacharia e(1964) ,Babe l(1968) ,FitzPatric k(1984) , Pawluk(1987) , andThompso n etal . (1990)hav epointe dt oth eoccasionall yver ylarg eportio no f enchytraeidexcrement si nmo ran dmode rhumu ssoils . Accordingt oToutai ne tal . (1983),thes eexcrement sar ever ypersistent ,an dma yestablis hparticulat elayer so n leaveso rneedles . Jegen (1920)an dKubien a(1955 )suggeste dtha tpotworm sma yproduc ea nex ­ tensive,b ei tspatiall y restricted,burro wsyste mwit ha spong yappearance . Singer& Krantz (1967)mentione da tendenc yo fenchytraeid si nlaborator y culturest otunne l throughth esubstrate . Gelder (1984)describe dth etunnelin gbehaviou ro f Lumbricillus lineatus; thesubstrat eha dt ob esufficientl y moistfo rth etunnelin gt ooccur ,an dth e tunnelswer estabilize dwit ha linin go fmucus . Górny(1984) ,o nth eothe r hand,state d thatterrestria lEnchytraeida ear eno tabl et oburrow . Invie wo fth e numerousauthor smentionin gminera lparticle sbein gtransporte db y enchytraeids,whethe rafte ringestio n (amongother sO'Connor ,1967 ;Babel ,1968 ; Matschek, 1972;Toutai ne tal. , 1983)o rattache dt oth ebod ysurfac e (Ponge,1984 )i t isreasonabl et oassum ea ninfluenc eo f potwormso nsoi lstructure . Ina fiel dexperi ­ mentwit hartificia lsoil sDidde n(1990 )wa sabl et osho wa significan t effecto f Enchytraeusbuchholzi o nai rpermeability ,por estructur ean daggregat estability , thoughth eamoun to fminera lsoi ltransporte d bythi sspecie sthroug hingestio nwa s verylo w(0.00 1- 0.01 % ofth etota lsoi l volume).

27 2.3.3. Microdistribution of Enchytraeidae

Generallysoi lanimal sexhibi ta contagiou s horizontaldistribution ,whic hma yb e correlatedwit hfactor s likemicroclimate ,th elocatio no ffood , ovipositionan dhatchin g ofeg gbatches ,intra -o rinterspecifi c attractiono rrepellency ,an dcompetitio n (Usher, 1976;Rougharden ,1977 ;Verhoe f &Va nSelm ,1983 ;Bradle y& Bradley , 1985). For theEnchytraeidae ,severa lauthor s haveexamine dthi spatter ni ndetai l(Nielsen ,1954 ; Peachey,1963 ;O'Connor ,1967 ; Matschek, 1972;Nakamura ,1979) . Nakamura (1979) analyzedth edistributio npatter no ffou rJapanes especie s(tw o Hemienchytraeus speciesan dtw oAchaeta species) usingth einde xo fpatchines san d the p-index(Iwao , 1972). Theseanalyse s revealeda genera ltren d inth especie sstud ­ iedt ocoalesc ei ncluster so f 200-400cm 2,th ecluster sthemselve shavin ga rando mt o slightlyregula r distribution. Whenth edat ao f Peachey(1963) ,fo rC . sphagnetorum, andO'Conno r(1967) ,fo ra populatio n dominated byMarionina cambrensis, are ana­ lyzedi nth esam eway ,thes eresult sar ecorroborated . Analyseso f Nielsen's(1954 ) data,fro m populationsdominate d byFridericia bisetosa, showtha tth esiz eo fth e clustersi nthi sspecie svarie dfro m 100-1000cm 2. Thedat ao f Matschek (1972)fo r Achaeta affinis suggestth eoccurrenc eo f rather compact (100cm 2) randomlydistrib ­ utedcluster s inthi sspecies . Intw oothe rstudie s Nakamura(1982,1985 ) established irregulartempora lpat ­ ternsi nth eaggregativ ebehaviou ro fAchaeta cameranian dHemienchytraeus bifurca- tus, respectively. Heck(1987 )als odemonstrate dappreciabl espatia lan dtempora l differences indegre eo fclusterin gfo rsevera lenchytraei dspecies . Itwoul dseem , therefore,tha tther ema yno tonl yexis t appreciablespecifi cdifference s insiz eo f enchytraeid clusters,bu tals ospatia lan dtempora lchange si nth edistributio npattern , probablyrelate dwit hheterogeneit y andchange si nbioti can dabioti cparameter s ofth e habitat. Theimportanc eo fenvironmenta lfactor si nth eformatio no fcluster swa s stressedb yChalupsk y &Lep S(1985) ,wh odemonstrate dth eoccurrenc eo fmulti - speciesaggregatio ncentre si nenchytraei dpopulations . Insom estudie s (Head,1967 ;Heungens ,1968 ;Wa y& Scopes , 1968;thi sthesis ) arelatio nwa sestablishe d betweenoccurrenc eo f potwormsan dth erhizosphere ,sug ­ gestinga connectio nwit hroo texudate san ddecayin g roots,eithe rdirectl yo rvi ath e microorganisms. Thisma yb eon eo fth ehabita tfactor s conducivet oth eformatio no f clusters. Theconsequenc e ofth especifi can dtempora ldifference s indistributio npatterns , istha tther ei sn oidea lsiz eo fsampl eunit st ob euse di npopulatio nstudies . Abraham- sen(1969 )an dAbrahamse n& Stran d (1970)arrive da tth esam econclusion ,bu tar ­ guedtha tth esiz eo fa sampl euni tshoul db esuch ,tha tth enumbe ro f unitswithou t enchytraeids arelow ,thu senablin gstatistica lanalysi so fth edata . Asa rule ,th evari ­ ationi nth edat aobtaine d decreaseswit hincreasin g sizeo fth esampl eunit s(Abraham -

28 sen,1969) ,bu tma yincreas eagai nabov ea certai nsiz e(La ie tal. , 1981). Generally, thesiz eo fth esampl eunit si schose na sa compromis ebetwee naccurac yo fth eresult ­ ingabundanc eestimate san dth eamoun to fwor kinvolved ,an dma yrang efro m1 0 cm2 (Springette tal. , 1970)t o4 2cm 2(Nielsen ,1955a) . Verticaldistributio no fenchytraeid s seemst ob emainl yrelate dt oorgani cmateria l inth eprofil eo nth eon ehand ,an dt ophysica lfactor so nth eother . Inmos tnatura l habitatsth elarges tpar to fth epopulatio noccur si nth euppe rlayers ,wher eth ebul ko f theorgani cmateria li slocate dan dmos to fth edecompositio n processestak eplace . In aGerma nbeec hfores t (Ellenberg etal. , 1986),mos tenchytraeid s occurredi nth e F-layerdurin gal lseasons ;her ecomminutio no flitte rwa sproceede dfurthest . The im­ portanceo fth elocatio no fsuitabl eorgani cmateria li scorroborate d byobservation si n ploughedagricultura lfields ,wher ea larg epar to fth epopulation sca nb efoun da tth e ploughingdept h(Lagerlö fe tal. , 1989;thi sthesis) . Physicalfactors ,notabl ysoi lmoistur e(Springet te tal. , 1970;Das h& Cragg, 1972a;Ellenber ge tal. , 1986)an dtemperatur e (Reynoldson,1939a ,b ;Peach - ey,1963 ;Das h& Cragg ,1972a ;Erman ,1973 ;Ellenber ge tal. , 1986),ma yinduc e verticalmigratio ni npotworms . Hondrue tal . (1971)reporte dtha ti nRumania nconifer ­ ousforest s enchytraeid speciesgroup scoul db echaracterize d byth eamplitud eo fthei r verticalmigrations . Especiallyi nextrem esituation slik edrough to rfrost ,i twill ,how ­ ever,alway sb equestionabl ewha tproportio n ofa nactua lvertica ldistributio n mayb e explainedb ydifferentia l mortality (O'Connor, 1957)an dwha tpar tb yvertica lmigration . Apartfromth edistributio no forgani cmateria lan dphysica lfactors ,th evertica l distributiono f potwormsma yals ob especie sdependent . Gröngröft &Miehlic h(1983) , forinstance , foundtha tCognettia sphagnetorum mainlylive di nth elitte r layeri nScot s pinestands ,Achaeta brevivasa occupyingth edeepe rlaye ran dMarionina clavata takinga nintermediat e position. Healy(1987 )recorde d1 3enchytraei dspecie si n an Irishquakin g marsh,mos to fwhic hwer econcentrate da tth esurface ,bu t Marionina riparia, Cognettiaglandulosa andthre eCernosvitoviella specieswer emor eabundan ti n deeperlayers .

2.3.4. Population dynamics

Intw oreview so nenchytraei decology ,O'Conno r(1967,1971 ) pointst osoi lmois ­ turean dtemperatur ea sdominatin gfactor si nth eseasona lfluctuation s inenchytraei d populations,eithe rdirectl yvi athei ractio no nth eanimal so rindirectl ythroug ha modifi­ cationo fthei renvironment . Inmois tsituation ssoi ltemperatur ewoul db edecisive ,i n periodso fdrough tmoistur ewoul db ea limitin gfactor . Thishypothesi swa sbase d mainlyo nresearc h byNielse n (1955b,c),O'Conno r(1957 ) andPeache y (1963),al l of whichwa sconducte d intemperat e regions. Sincethen ,mor epopulatio ndynamica l

29 studieshav ebee nconducted ,rangin gfro marcti chabitat s (Solh0y, 1975)t otropica l soils(Thamb i& Dash ,1973) . Inmos tcase sth egenera ltren di nth eseasona lvari ­ ationsi nnumber san dbiomas scorroborate dth eassumptio no ftemperatur ean dmois ­ turebein go fprimar yimportanc efo rpopulatio ndynamics . Yet,ther ear ea numbe ro findications ,som eo fwhic hhav ebee nmentione d above,tha tthes etw ofactor sd ono tsuffic et oexplai nseasona ldynamics . Ina stud yo f theenchytraei dpopulation s inNorwegia nconiferou sforests ,Abrahamse n(1972 ) found,apar tfro ma correlatio nwit hsoi lmoisture ,a correlatio nbetwee nth etyp eo f vegetationan dth etim eo foccurrenc eo f populationmaxima . Ina numbe ro fstudie s deviationsfro mexpecte dpopulatio ndevelopmen twer erecorded , withenchytraei d populationsgrowin gi nunfavourabl emoistur ean dtemperatur econditions ,o rdeclinin g infavourabl econditions . Examplesar ePeachey' s (1963) Nardus-site,a mois thabitat , wherea pea ki npopulatio ndevelopmen toccurre dsubstantiall y latertha ni ncompa ­ rablesite si nth esam estudy ,an da Germa nspruc efores t (Gröngröft, 1981; Gröngröf t &Miehlich ,1983) ,wher ei ncontinuousl ydr yconditions ,afte r aninitia ldeclin e in abun­ dance,a considerabl e populationgrowt hwa srecorded . Another indication isfoun di n theexperiment s of Matschek (1972),wh ounsuccessfull ytrie dt oincreas eafiel dpopu ­ lationo fAchaeta affinis bymanipulatin gsoi lmoistur econten tan dtemperature . In population dynamicalstudie swher eenchytraeid sar eidentifie dt ospecies ,ofte ninter ­ specificdifference s indynamic sar erecorde d(Möller ,1967 ;Dózsa-Farkas ,1973b ; Klungland,198 1; Gröngröf t& Miehlich ,1983) . Observations likethes esugges tth e existenceo f intraspecificadaptation st oenvironmenta lstress ,resultin g inmor e com­ plexmechanism sdeterminin gpopulatio ndevelopment . Someo fthes eadaptation s may be: - Enteringa ninactiv estat eunde radvers econditions . Cocoonsar ea nexampl eo f sucha ninactiv estate ,offerin gth eembryo sprotectio nagains tadvers econditions . Willard (1972)foun denchytraeid s indiapaus ei ndr yperiod san dmentione dtha ti n thisstat ethe yapparentl y neededsom etim et obecom eactiv eagain . Dózsa- Farkas(1973b,c )describe da simila rbehaviou ro fStercutus niveus, wheredurin g thesumme r monthsth eanimal sliv ei nsmall ,dense ,inactiv ecluster si nth e deepersoi llayers ,eve n underfavourabl etemperatur ean dmoistur econditions . Ivleva(1969 )describe dth eformatio no f densecluster s (synaporia) of Enchytraeus albidus infloode dconditions ,an dmentione dthi sa sa norma lreactio n inthi s speciest oenvironmenta l stress. Adaptations likethi sma yresul ti nsmalle rnum ­ berso fworm scounte ddurin gcertai npart so fth eyear ,throug ha lowe rextractio n efficiency ora mor econtagiou sdistribution . Whensuc hinactiv estage swoul dbelon gt oth ephenolog yo fa species ,a si nth e caseo fS. niveus, thiswoul dresul ti nrecorde dabundance sdevelopin gagains tex ­ pectationstha tar ebase do nvalue so f physicalfactors . Indicationsfo rthi sar e reported,amon gothers ,b yO'Conno r(1967 )an dKlunglan d (1981),wh osug ­ gestedtha treproductiv eactivit y (cocoonproductio nor ,i nth ecas eo f Cognettia

30 sphagnetorum, fragmentation) wouldmainl ytak eplac ei nautumn ,th ecocoon so r fragmentswoul dhibernat ean dtha tpopulatio ndevelopmen t insprin gwoul dresul t frommas shatchin g andregeneratio no ffragments . Iti sclea rtha t more, experi­ mentallyobtaine d informationo nthi ssubjec twoul db e desirable. Acceleration orretardatio no fth ereproductiv ecycl ea sa respons et o environ­ mentalconditions . Giere& Hauschild t(1979 ) reporteda larg evariabilit y inth e lengtho fth evariou sphase so fembryogenesi si nLumbricillus lineatus. Thus , underunfavourabl e conditionsdevelopmen to fth eegg sma yb eretarded ,leavin g theembryo si nth eprotectio no fth ecocoon . Inmor efavourabl esituation spopula ­ tiongrowt hma yb eexplosive ,a sa resul to fth ecombine deffec to facceleratio no f embryogenesis andsimultaneou s hatchingo fcocoons . Iti squit econceivabl etha t sucha mechanis m mayoperat ei na numbe ro fenchytraei dspecies .

2.3.5. Production ecology

Thedirec tcontributio no fpotworm st oenerg yan dmatte reconomic si nterrestria l ecosystems isreflecte d inthei rconsumptio n andassimilatio no forgani cmaterial . Indirecteffect s onth eflow so fenerg yan dmatte roccu rthroug hfeedbac k mechanisms toothe rtrophi clevel s inth esoi lcommunit yan dinfluence so nchemica lan dphysica l habitatproperties . Asth edirec tcontributio no fa taxo nt oth efunctionin go fth edecompose rsubsys ­ temca nno tb edetermine dempiricall y underfiel dconditions ,i ti squit ecommo nt o makeestimate sbase do nstandin g stockfigure san dgeneralization s aboutpopulatio n biologyan dphysiologica lcharacteristics . Acommonl yuse dapproac hi sbase do nth e amounto f energy utilizedb ya population ,th eassimilatio n (Petrusewicz& Macfadyen,1970 ;Hea l& MacLean ,1975) . Asomewha tdifferen t approachconcen ­ trateso nth ecyclin go fnutrients ,an dtrie st oquantif yth eamoun to fnutrient strans ­ formedb ya population. Petrusewicz &Macfadye n (1970)propose dth ecommonl yuse denerg ybudge t equationsC = A + F and A= R + P , where: Consumption, theamoun to fenerg yconsume d A=assimilation,th eamoun to fenerg yuse d R=respiration,th eamoun to fenerg yuse dfo rmaintenanc e P=production,th eamoun to fenerg yuse dfo rtissues ,cocoon san dexcreta . F=defecation,th eamoun to fenerg ysecrete do rexcrete d

Asfo r respiration,som eexperimentall yobtaine ddat aexis tfo r severalenchytraei d species (Nielsen,1961 ;O'Connor ,1963 ;Standen ,1973) . Asthes edat awer eob ­ tainedunde rlaborator yconditions ,wit hth eworm s beingrathe r inactive,actua lrespira -

31 tion infiel d conditions probablywil l be higher (Wightman, 1977); Hutchinson & King (1980) suggested thatfactua l respiration of Enchytraeidae may be even 20% higher. Nevertheless, the experimentally obtained data have been used bysevera l authors (Reichle, 1971;Persso n & Lohm, 1977; Phillipson et al., 1979) to construct common respiration equations for Enchytraeidae, which are widely beingapplied . Using an estimate of respiration,th e other parameters inth e energy budget may be obtained by applying estimates of the ecological efficiencies A/C and P/A (Heal & Maclean, 1975), or, alternatively, by using estimates of relative productivity (P/B, where B=biomass of the population) (Standen, 1980a; Makulec, 1983) and consumption (McBrayer& Reichle, 1971). Table 2.2 lists mean biomasso f Enchytraeidae, estimated respiration and the proportion of total soil respiration accounted for byenchytraeids ,fo r a number of habi­ tats acrossth e world. Biomassfigure s originally presented asfres h weight were con­ verted todr yweigh t usingth efres hweighl/dr yweigh t ratios mentioned byth e author (rangingfro m 5.0 [Standen, 1984] to 7.69 [Ryl, 1977,1980]), orth e value of 5.56 (Ed­ wards, 1967) where nofres hweight/dr yweigh t ratiowa s mentioned. The proportiono f total soil respiration accounted for by potwormswa s either taken from the publication, orwa s expressed as a percentage of the energy content of the litterenterin g the soil (MacFadyen, 1963), if mentioned. Although considerable differences instandin g crop and respiration were recorded,thes e data suggest thatth e direct contributiono f enchytraeids to total soil respiration can be small but significant in all habitats. Highest values are reportedfo rforests , but lowvalue sfro m this habitatfal lwel l below the higher ones inth e other habitats. Proportions range from 0.3% to 3.4% of the total soilrespi ­ ration, butgenerall y not more than 2% of the energy transformations can be attributed directly topotworms .

The construction of an energy budget allows propositions to be made onth e pro­ portion of the energy inth e primary production utilized by enchytraeids. When the focus iso nth e cycling of nutrients, however, the contribution of potworms may even be more important, as a concentration of several nutrients, notably nitrogen and phospho­ rus, takes place from plant material via microbialt o enchytraeid tissues, as is illustrated in Table 2.3. Enchytraeids may therefore, like soilfaun a in general (Swift, 1977; Pokarzhevsky et al., 1989) playa n important role inth e turnover of nutrients. The amount of nutrients stored inenchytraei d tissue at any one timewil l be a significant parameter here. A noteworthy point inthi s respect istha t production efficiency isin ­ versely related totemperature , causing relatively less nutrientst o be stored in enchytraeid tissue at higher temperatures. The composition of the food assimilated will also play a substantial part, butdat a on this subject are largelylacking .

Besides the direct effect of potworms on decomposition processes, there are indirect effects, that may resultfro m enchytraeid influence on the microbial community

32 Table 2.2:Average biomassand production-ecological dataof Enchytraeidaein various habitats.

Biotope Country iiomass Respiration Percentage of Production Author(s) (gd.w/m 2) (kJ/mfy) total soil (kJ/m2/yr) respiration

Grassland

arctic meadow Canada 0.59 10.7 0.3 13.0 Ryan, 1977;Whitfield , 1977 raised beach Canada 0.18 6.8 1.5 8.1 sedge meadows Alaska 0.38 97.1 2.8 120.5 MacLean, 1980 tropical India 0.02 <1.0 >1.2 Dash et al., 1974 grazed, 10sheep/h a Australia 0.12 143.0 1.1 Hutchinson & King, 1979 grazed, 10 sheep/ha Australia 0.10 110.1 1.9 Hutchinson & King, 1980 grazed, 20 sheep/ha Australia 0.05 62.4 1.0 grazed, 30 sheep/ha Australia 0.04 44.0 1.8 grazed meadow England 2.16 427.4 2.0 Macfadyen, 1963 hay meadows England 1.76 77.4 Standen, 1984 meadow Poland 0.26 132.3 Ryl, 1980 pasture, dry Denmark 0.53 148.0 Nielsen, 1961 pasture, mesic Denmark 0.55 193.8 pasture,we t Denmark 1.89 651.8 ley Sweden 0.34 56.3 0.5 37.5 Lagerlöfetal., 1989 lucerne ley Sweden 0.54 108.4 0.9 72.3

Moor

spruce swamp Finland 1.73 500.3 Hotanen, 1986 pine bog Finland 0.09 24.7 blanket bog England 2.38 262.0 2.0 48.0 Standen, 1973

Forest

deciduous, oak The Netherlands 1.60 251.4 1.8 Van Der Drift, 1974 deciduous England 3.96 700.0 2.7 Satchell, 1971 deciduous, beech England 0.34 85.6 1.6 Phillipsonetal., 1979 deciduous, beech Germany (FRG) 1.64 334.9 2.6 502.4 Ellenberg et al., 1986 deciduous, beech Germany (FRG) 1.31 369.2 3.4 95.0 Römbke, 1988 deciduous, beech Germany (FRG) 0.42 116.8 1.4 43.8 Meitin, 1988 deciduous, beech Germany (FRG) 0.60 177.0 1.3 70.0 Schaefer, 1990 deciduous Japan 0.44 164.8 2.1 Kitazawa, 1971 Liriodendron forest USA 0.50 156.6 0.6 Reichte et al., 1975; 1977 deciduous, ash-alder Poland 0.32 71.0 0.9 47.3 Makulec, 1983 deciduous, oak-hornbeam Poland 0.43 87.6 1.6 58.4 mixed, pine-oak Poland 0.45 104.2 1.9 69.5 coniferous, pine Poland 0.39 80.3 1.7 53.5 coniferous Wales 1.94 626.4 O'Connor, 1963 coniferous S-Finland 0.23 30.8 0.6 Huhta & Koskenniemi, 1975 coniferous N-Finland 0.17 8.1 0.3 coniferous Sweden 0.46 103.2 0.9 Lundkvist, 1982 coniferous, subalpine Japan 1.17 383.4 1.6 Kitazawa, 1977 coniferous, subalpine Japan 0.20 48.3 0.6 Kitazawa, 1971 subtropical rainforest Japan 0.20 176.1 0.8

Arable land

barley Sweden 0.59 109.3 1.5 73.0 Lagerlöfetal., 1989 lucerne Poland 0.17 54.4 Ryl, 1980; rye Poland 0.11 61.1 0.9 Golebiowska et al., 1974 sugar beeVwheat Poland 0.51 77.9 potato Poland 0.32 134.8 0.4 winter wheat The Netheriands 0.20 58.8 0.8 39.2 this thesis sugar beet The Netherlands 0.55 241.2 3.2 160.8

33 Table2.3: Nutrient concentrations (percentage dry weight) inlitter, microbial and enchytraeid material. Legend to authors: 1: Zaboev et al., 1987;2: Borkott, 1989;3: Nielsen, 1961; 4: Olechowicz & Mochnacka-Lawacz, 1985; 5: Heal et al., 1978; 6: Swift, 1977; 7:Krivolutzky& Pokarzhevsky, 1977;8: Flanagan & Van Cleve, 1977;9: Tischler, 1965; 10:McKercheretal., 1979; 11: Pokarzhevsky etal., 1989; 12:Ausmus& Witkamp, 1973; 13:Cromacketal., 1975.

Nutrient Plant material Bacteria Fungi Enchytraeidae

9 11 12 Nitrogen 0.44-3.025 4-12 ' ' 13.g 6,8,9 5.3-13'**•" Phosphorus 0.013-0.165 0.9-3.011>12 0.09-1.06811 0.32-1.62410'1 Potassium 0.013-0.35'7 1.5-11.5 "•" 0.12-4.0 " 0.6-0.82A" Calcium 0.08-0.85 " 0.95 '2 0.07-3.3,ws 0.22-0.51 "7 Magnesium 0.031-0.53 " 0.1512 0.07-0.1961213 0.11-0.44'7 andit sactivity ;vi acomminutio no forgani cmaterial ,mixin go iorgani cmateria lwit hth e soil, (selective) grazing onmicroorganism s anddispersa lo f spores,(amon gothers : Toutaine tal. , 1982;Ponge , 1984; Toutain,1987 ;Wolters ,1988) . Indirecteffect sma y alsoresul tfro mselectiv eimmobilizatio n orexcretio no f nutrientslik eCa " (Andersone t al., 1983). Sucheffect s arever ydifficul tt oquantify ,bu tar ewithou tdoub to fmajo r importancei nan yecosyste mwit ha nappreciabl epopulatio n ofenchytraeids . An indicationfo rthi swa spresente d byDózsa-Farka s (1978b),wh ocalculate dtha tu p to 6.9%o fth ehornbea mlitte r producedi nHungaria nhornbeam-oa kforest spasse d throughth egu to fth eenchytraei dspecie sFridericia ratzeli and F.galba. Abrahamsen (1990)establishe d ina microcosm-experimen ttha tth epresenc eo f C. sphagnetorum enhancedN-mineralizatio nb y18 %o naverage . About40 % ofthi sdifferenc epresuma ­ blyoriginate dfro mdecomposin genchytraei dtissue . Wolters (1988)demonstrate dtha t theeffect s ondecompositio n processeso fMesenchytraeus glandulosus depend on factorslik epopulatio n densityo fth eenchytraeids ,temperature ,growt hcondition so f themicroflora ,an dth ecompositio n ofth emicrobia lcommunity . Differences between enchytraeid species asregard sthei rfeedin gactivit y and foodpreferenc emus tb etake n intoaccount , however, inassessin gthei rfunctio ni ndecompositio n processes(Dózsa - Farkas,1982) .

34 2.4.Concludin gremark s

Thelon ghel dvie wo fterrestria lenchytraeid sa sbein ga rathe r uniformgrou p of speciesa sregard sthei rreactio nt ophysica lo rbiologica lfactor sseem st ob eobsolete . Therear eman yindication sfo rappreciabl einter -an dintraspecifi cvariatio nwithi nthi s oligochaetefamily . Itma yb econclude dtha tth eEnchytraeida esho wa smuc h ecologi­ calvariet ya san yothe rfauna lgroup . Thisbring sth enee dfo recologica lresearc ha t thespecie slevel . Basictopic st ob eaddresse di nthi srespec tare : - Thetaxonom yo fthi sgroup ,whic hbadl yneed srevisio nan delaboration ,sinc eth e numbero fspecie san deve ngener ai seve rincreasing ,an dconfusio na sregard s theidentit yo f speciesi sa commo nproblem ,especiall y inth ewidesprea dgener a Enchytraeus, Fridericia and Marionina. - Theculturin go fenchytraeids ,a sunti lno wonl yspecie sfro mth egener a Enchytraeus andLumbricillus canb eculture di nsufficien t numberst ob euse di n ecologicalexperiments .

Theimportanc eo f Enchytraeidae inth efunctionin go fterrestria lecosystem si s becomingincreasingl yclear . Yet,fo ra goo dunderstandin g ofthei r role,an da quanti ­ tativeevaluatio no fth efactor sinfluencin gpopulatio ndynamic san dactivity ,severa l pointsurgentl ynee dfurthe rstudy ,notably : - Ananalysi so fth ephysiologica lan dbehaviora ladaptation so fenchytraei dspe ­ cies,whic hma yb eo fmuc hhel pi npredictin gth eimpac to fchange si n environ­ mentalcondition so nenchytraei dpopulations . - Theinteraction s betweenenvironmenta lfactor s (soilfactors ,xenobiotics ) inthei r effecto nenchytraei dpopulations ,a si ti sclea rtha tth eeffec to fan ysingl efacto r willals ob edetermine db yothers . - Prédationan dparasitis m undoubtedlyinfluenc eenchytraei dpopulatio nsizes . Quantitativeevaluatio no fthes eeffect s maycontribut et oth eunderstandin go f their populationdynamics . - Thefeedin g biologyo fenchytraei dspecie si sa fiel dwher ea lo to fwor kha st ob e done,befor eth efunctionin go fenchytraeid s insoi lsystem sma ysatisfactoril yb e described. Therema yexis tsevera lfeedin gstrategie samon gpotwor m species, buta sye tonl yver yfe wspecie s havebee ninvestigate di nan ydetail ,an dinsigh t inth eimpac to fenchytraei dfoo drelation s islargel ylacking .

Progress inthes efield swil lb ever yusefu lfo rth eunderstandin go fecosyste m functioning,an dfo rth edevelopmen to fecologicall y soundmanagemen t practices,bot h innatura lan dagricultura lecosystems .

35 3. Population dynamicsan d production ecology of Enchytraeidae inhig han d reduced inputfarmin gsystem s

Abstract

Populationdynamics ,productio n ecologyan drol ei nnutrien tcyclin go f Enchytraeidaewer estudie di na 'conventionally ' (withhig hinpu to fenerg y andmatter ) managedarabl efield ,alon gwit hthre efield swit hvariou s'inte ­ grated' (withreduce dinput ) managementtypes . Meanenchytraei dabun ­ dancean dbiomas srange dfro m1100 0ind/m 2 to4300 0ind/m 2 and from 0.08 gC/m 2t o0.4 2g C/m 2respectively . Itwa scalculate dtha ti nth e conven­ tionallymanage dfiel d1.0 2 -2.58 %o fth eorgani ccarbo ninpu twa srespire d byth eenchytraeids ,i nfield swit hintegrate d managementthi swa s 0.52- 3.73%. Nitrogenflu xfro mth epopulation swa scalculate dt orang e from0.1 9 -0.60g N/m 2/yr. Ingenera l nosignifican tdifference s inseasona ldynamics ,mea nabundanc e andbiomas soccurre d betweenth einvestigate dfields . However,a pro­ nounceddifferenc e betweenth efiel dmanage dconventionall y andth efield s withintegrate d managementwa sfoun da sregard svertica ldistributio n ofth e enchytraeids. Therear estron gindication stha tth evertica ldistributio nwa st o alarg eexten tinfluence db ysoi ltillag e andth edistributio no fenchytraeid s coincidedwit htha to f organicfertilize r andplan tresidues . Duringth egrowin g season,th eenchytraei ddistributio nwa sals oinfluence d byth epositio n ofth ecro pplants ,indicatin ga nassociatio no fth eenchytraeid s withroo texudates .

3.1. Introduction

Thepresen tstud y ispar to fth eDutc hProgramm eo nSoi lEcolog yo fArabl eFarm ­ ingSystems ,whic hstarte di n 1985.Th eprogramm efocuse so nth eregulator ymecha ­ nismso fth epool san dflow s ofcarbo nan dnitroge ni nth esoil ,an do nth e interactions betweensoi lorganism san dsoi lstructure . Soilbiology ,soi lphysic san dsoi lchemistr y andmeteorologica l parametersar emeasure di nhig han dreduce dinpu tfarmin gsys ­ tems. Conventionalagricultur ei nth eNetherland s isconsidere d ahig hinpu tsystem . Inreduce dinpu t (integrated) systems,nutrien tinputs ,soi ltillag ean dus eo fbiocide s arecu tdown ,an dbiologica lprocesse s andinteraction sar eexpecte dt ob emor eimpor -

36 tant(Brussaar de tal. , 1988;Kooistr ae tal. ,1989) . Withinth eframewor ko fthi sprogramm e Enchytraeidaear estudie dwit hrespec tt o nutrientcyclin gan dsoi lstructur eformation . Resultso nenchytraei dinvolvemen t insoi l structureevolutio n havebee npublishe delsewher e(Didden ,1990) . Here,th edat aar e presentedo npopulatio ndynamics ,respiration ,productio nan dnitroge nturnove ro fth e enchytraeidpopulation s infou ro fth efield sunde rstudy . Kasprzak (1982)reviewe dth eexistin ginformatio no nnumber san dbiomas s of Enchytraeidae inagricultura lsystems ,mainl yfro mPoland ,Swede nan dDenmark . Sincethen ,severa lmor estudie shav eappeare d(Andre n& Lagerlöf ,1983 ;Lagerlöf , 1987;Parmelee ,1987 ;Lagerlö f etal. , 1989). Fromth eavailabl edat ai tappear stha t enchytraeids mayconstitut ea significan t mesofaunagrou pi nagricultura lecosystem s oftemperat eregions ,an dtha tagricultura lpractic ema yconsiderabl yinfluenc especie s composition,number san dbiomass . Asth eimportanc eo f Enchytraeidae innutrien tcyclin gwa ssuppose dt ob erelate d withpopulatio ndevelopment ,specie scomposition ,an dactivit yan ddept hdistributio no f thepopulations ,a detaile dpopulatio n studywa scarrie dou tove ra thre eyea rperiod . Tob eabl et orelat emanagemen taspect st ocharacteristic s ofenchytraei dpopulations , fourarabl efields ,differin g inmanagemen tand/o r history,wer einvolved . Thedat ao f thepopulatio nstud ywer eals ouse dt ocalculat e respiration,productio nan dnitroge n flowsfo rth eenchytraei dpopulations ,an dth erelativ eimportanc eo fenchytraeid s inth e foursystem s understudy .

3.2.Method san dmaterial s

3.2.1. The experimental site

Thefiel dwor kfo rthi sstud ywa scarrie dou to nth eexperimenta lfar m'Dr .H.J . Lovinkhoeve' inth eDutc h Noordoostpolder, reclaimedi n1942 . Thesoi li sa sil tloam , witha sil tfractio n (particles< 1 6jum )o fabou t30% , 10%calciu mcarbonat ean da p H (KCl) of7.5 . Ata dept ho fapproximatel y2 5c mth etextur echange sint over yfin e loamysand .Th eyearl yrainfal li s65 0- 80 0mm . Croprotatio n since198 5consist so f winterwhea t- suga rbee t- sprin gbarle y- potatoes . Typeso ffar mmanagemen trepre ­ sentedare :conventiona l (tillagedept h2 5cm ,hig hinpu to ffertilizer s ando fpesticides) , integrated (tillagedept h1 5cm ,5 0- 70 %o fconventiona lfertilize r use(dependin go n crop),gree nmanure ,lo wamount so fpesticides ) andintegrate dwit hminimu mtillag e (tillagedept h5 cm). Thesamplin gcomprise dth eperio dMa y198 5t oan dincludin gApri l 1988. Four fieldswer einvolve di nth esamplin gprogramme :on econventiona lfield ,tw ointegrate d

37 fields (inthi stex treferre dt oa s'integrate dI 'an d'integrate d II')an don eintegrate dfiel d withminimu mtillag e(referre dt oa s'Minimu mtillage') . Twoo fthes efield swer e in-

Table3.1 Characteristics of tf?e four sampled fields (after Kooistra et al., 1989).

Field Conventional Minimumtillag e Integrated I Integrated II

Management: previous* Crop residues only Crop residuesplu s Crop residuesplu s Crop residuesonl y (since 1953) green manures green manures,organi c manures, and leys present Conventional Integratedwit h Integrated Integrated minimum tillage since 1985 1986 1985 1985

Crops: 1984 Potato Potato Potato Winter wheat 1985 Sugar beet Sugar beet Sugar beet Rax 1986 Winter wheat Springbarle y Winter wheat Winter wheat 1987 Sugar beet Sugar beet Sugar beet Sugar beet

Organic matter (%): 0-10cm 2.09 2.35 2.67 2.26 10-25 cm 2.12 2.37 2.81 2.32 25-40 cm 1.90 2.32 2.07 1.87

sampledfrom : May 1985 May198 7 May198 5 May 1987

*:contemporary Dutchtillag edept han dpesticid euse ; organicaddition s asindicated .

eludeda ta late rstag eo fth esamplin gprogramme . Table3. 1 liststh echaracteristic s ofth efou rfields . Organicmatte rinpu t(organi c fertilizer and cropresidues )wa sestimate dt ob e14 0g C/m 2/yri nth econventiona lfiel d and21 0g C/m 2/yri nth eothe rfields . Atth efar mai rtemperatur ean dprecipitatio nwer erecorde ddaily . Forsoi ltem ­ perature,us ewa smad eo fdat afro m10,2 0an d5 0c mdept ha tD eBil t(Roya lDutc h Meteorological Institute,circ a8 0k m fromth eexperimenta l site),a sdat ao nsoi ltem ­ peraturea tth eLovinkhoev eexperimenta lsit ewer eno tsystematicall ycollected .

3.2.2. Sampling procedure

Enchytraeidswer esample da tmonthl yintervals ,unles sthi swa sno tpossibl eb y fieldcondition ssuc ha shig hrainfall ,o rwhe nlarg eenchytraei d numbers causeda prolongedelaboratio ntim efo rth esampl eunits . Perfiel dpe rsampl edat e6 -1 0core s weretaken . Theprocedur efollowe d arando msamplin gdesign ,excep tdurin gth e growingseason ,whe nth esampl eunit swer edistribute dwithi nan dbetwee nplan trows . A4 0c mlon gstee lspli tcore rwa sused , containing2. 5c mhig hplasti cring swit h

38 aninne rdiamete ro f6 cm . Upt oJul y 1986samplin gdept hrange dbetwee n2 5an d 32.5cm ,afterward s itwa s4 0cm . Thecore swer edivide di n2. 5c mslice si nth elabo ­ ratory. Extractionwa scarrie dou taccordin gt oO'Conno r(1955) ,wit happlicatio no f increasingligh tan dhea thal f anhou rafte rth estar to fextractio nan da tota lextractio n timeo f3 hours . Thecollecte danimal swer eexamine daliv eunde ra microscope ,measure dt oth e nearestmm ,an didentifie dfollowin g Nielsen& Christense n (1959,1961,1963)an dth e availablemor erecen tspecie sdescriptions . Presumablyne wspecie swer eassigne d bycharacters . Foral lspecimen sth elif estag ewa srecorde da sjuvenil eo radult . FromMa y198 5t oan dincludin gOctobe r 1985,henc ebefor eth estar to fth e pres­ entmanagemen ttype ,samplin gwa sles sdetailed . Notal lslice si na sampl euni twer e extractedan dth eextracte dpotworm swer eno tidentifie dt ospecie s(Marinissen , un­ published). Tob eabl et ous eth e198 5sample stogethe rwit hth esubsequen tsamples , linearregressio nwa suse dt oestimat enumber san dbiomas so f animals inslice stha t hadno tbee n extracted.

3.2.3.Analysi s of the data

Forth eanalysi so fth edat aan dpresentatio no fth eresults ,th esoi lprofil ewa s dividedi n4 sub-layers :0 - 5 cm ,5 -1 0cm ,1 0- 2 5cm ,an d2 5- 4 0 cm. Thesamplin gdat awer estatisticall yanalyze d usinganalysi so fvarianc e(afte r logarithmictransformatio n ofth edata )an dusin gdistribution-fre emethods . Canonicalcorrespondenc e analysis(progra mCANOCO ,Te r Braak, 1987)wa s usedt oanalyz eth erespons eo fabundanc ean dbiomas so fth evariou sspecie san d of theenchytraei d populationsa sa whole ,t oquantitativ eenvironmenta lvariable s(suc h astemperatur e andprecipitation ) andqualitativ eenvironmenta lvariable s (sucha s managementtype) . Thedept hdistributio no fth eenchytraei dpopulation swa s evalu­ atedi nthes eanalyse sb ytreatin geac hspecie sa sfou rdifferen tspecies ,on efo reac h sub-layerdiscerne d inth esoi lprofile . Asth etim etha telapse dfro msamplin gtil lex ­ tractiono fa sampl euni tcoul db eo f someinfluenc ei nth eanalyses ,i twa sinclude da s acovariable .

3.2.4. Production ecological calculations

InMa yan dJun e 1987an dJanuar yan dFebruar y198 8a numbe ro fenchytraeid s fromth efiel dsamplin gwer efreeze-dried ,an dthei r individualweight sdetermine do na Cahnelectrobalance . Assuming apowe rfunctio nt ogiv eth ebes tfi tfo rth edat a(Abra - hamsen, 1973),linea rregressio n equationso f lengtho nweigh twer ecalculate d (after logarithmictransformatio no fth edata )fo rth especie soccurrin ga tth eLovinkhoev e

39 experimentalsite . Theseequation swer euse dt ocalculat eth estandin g cropo f enchytraeids. Toestimat eth estandin gcro pi n1985 ,i twa sassume dtha tth especie scomposi ­ tioni nth evariou slayer so fth esoi lprofil ewa sth esam ea sth eaverag especie scom ­ positioni nth enex tyears .

Respirationwa scalculate dfro mth estandin gcro pestimate san dth edat ao nsoi l temperature,applyin gth eapproac ho f Perssone tal . (1980),wh ouse dth eformul a Q=33.6W°67, where 3 1 1 Q= mm 0 2 ind hr W= bod yweigh t (gfres hweight ) Thesam eauthor suse da fres hweight/dr yweigh trati oo f6.6 7an da Q1 0o f2 above5'C ,assumin ga linea rdecreas e inoxyge nconsumptio nt ozer oleve lbetwee n 5°Can d-5'C . Foreac henchytraei dspecie soccurrin g inth efield ,a linea rcours ei n numbersi never ylengt hclas sbetwee nsamplin gdate swa sassumed . Soil tempera­ tureswer etake nt ovar ylinearl ybetwee nth evariou sdepth so f measurement (withai r temperatureprevailin ga t1 0c mabov eground) . Inthi swa yestimate so frespiratio nfo r theenchytraei dpopulation swer ecalculate do na dail ybasi sfo rvariou sdepths . Consumptionan dproductio nwer ecalculate dfro mth erespiratio ndata . Useo fth e efficiencyquotient s proposedb yHea l& MacLea n(1975) ,assumin genchytraeid st ob e 20%saprovorou san d80 %microbivorou s(Whitfield ,1977 ;MacLean ,1980) ,resulte di n thefollowin gefficienc yquotients :P:C=0.112an dR:C=0.16 8(P=production , C=consumption,R=respiration) . Consumptionan dproductio nwer eexpresse da s amountso fC o rN . AC-conten to f4 1% (dw )wa sassume dfo rorgani cmatte r inputi n thefiel dan do f50 % (dw)fo renchytraeid s (Lundkvist, 1982;Borkott , 1989). N-content (dw)o fenchytraeid swa stake nt ob e13 %fo r Fridericiaspecie san d1 1% forothe r species (Nielsen,1961 ;Lundkvist , 1982;Borkott ,1989) . N-fluxfro menchytraei dtissu ewa scalculate d usingth edail yfigure so nstandin g cropan dproduction . Ane tincreas eo fnitroge ni nenchytraei dtissu ewa stake nt o occur, whena nincreas ei nstandin gcro pequalle do rexceede dcalculate dproduction . Inothe rcase si twa sassume dtha ta ne tdecreas eo fth eamoun to f nitrogentoo kplace .

Thedat awer ecompare do na year' sbasis . Thedat afo rConventiona lan dInte ­ gratedI i n198 7wer euse dt oestimat e numbersan dbiomas sfo rth eperio dJanuar yt o Mayi n198 5(fo rConventiona lan dIntegrate d I)an d198 7(fo rIntegrate d IIan dMini ­ mumtillage) ,fo rwhic hdat awer elacking .

40 3.3.Result s

3.3.1. Composition ofth e enchytraeid fauna

Table 3.2 lists the proportional composition ofth e enchytraeid fauna in numbers and biomass and the mean diversity and evenness inth e upper 40 cmo fth etwo , respectively four investigated fieldsfo rth etw o years ofdetaile d sampling.

Table3.2: Proportional abundance (A) and biomass (B) per year of the variousenchytraeid species inthe upper40 cm of the investigated fields and mean diversity (Shannon's entropy) and evenness(Hurlbert, 1971)in the period May to and including April of the next year.

Species Conventional Minimumtillag e IntegratedI IntegratedI I

1986 A B A B

Enchytraeusbuchholzl 55.57 30.07 71.20 33.85 Henleaperpusilla 10.63 9.42 5.99 6.01 Henlea ventriculosa - - 0.87 2.28 Buchholzia appendiculata 5.47 6.25 0.52 0.81 Frideridabulboides - - 0.74 1.26 Fridericia sp.A 4.19 10.74 13.42 40.30 Fridericia sp. B 13.55 35.93 3.58 11.46 Fridericia sp. C 10.58 7.59 3.50 4.00 Marionina sp. - - 0.17 0.04 No. ofspecie s 6 9 Diversity 1.06 0.92 Evenness 0.64 0.47

1987 A B A B A B A B

Enchytraeusbuchholzi 63.06 28.53 47.59 20.11 67.63 28.17 36.10 16.08 Henleaperpusilla 5.90 5.41 15.28 15.59 8.21 7.67 20.15 23.37 Henlea ventrkulosa 5.08 11.37 0.95 3.16 4.83 26.53 0.19 1.81 Buchholzia appendiculata 1.66 2.37 11.62 10.64 3.20 4.58 16.67 15.59 Fridericia bulboides 0.49 0.54 1.86 2.09 1.03 1.90 15.72 16.60 Fridericia sp. A 1.48 4.07 3.52 9.78 9.17 21.84 9.24 23.73 Fridericia sp. B 15.54 42.33 15.08 35.38 3.48 6.86 1.44 2.61 Fridericia sp. C 6.78 5.37 4.09 3.24 2.35 2.46 0.45 0.20 Marionina sp. - - - 0.11 0.01 0.04 0.00 No. of species 8 8 9 9 Diversity 1.05 1.36 1.24 1.43 Evenness 0.63 0.71 0.60 0.69

Intota l9 specie s of Enchytraeidae were recorded;th e lowest number (6) ofspe ­ cies occurred inth e conventional field in1986 . Inal lfield s was the most abundant species,wit h Henleaperpusilla and Fridericia species being second in abundance. Asregard s biomass,£ buchholzi was, due toit scomparativel y small size, not dominating; Fridericia species generally accountedfo rth e larger part ofth e biomass.

41 Diversitywa slo wi nal lfields ,a swa sevenness ,reflectin gth elo wnumbe ro f speciesan dth enumerica ldominanc eo f E.buchholzi. In198 7diversit yi nIntegrate dI wassignificantl y increaseda soppose dt o 1986( P< 0.05 ,Mann-Whitne ytest) . Forth e conventionalfiel dthi swa sno tth ecase ;i n198 7thi sfiel d hadlowes tvalue sfo rdiversit y andevennes so fal lfou r investigatedfields ,th edifference s indiversit ywit hMinimu m tillagean dIntegrate d IIbein gsignifican t (P< 0.0 5an dP < 0.0 1 respectively,Mann - Whitneytest) .

3.3.2.Vertica l distribution and relation to plant position

Conventional L n

760C Ê25 _o .c Apr 18 May 3 Jun 19 Jul 16 Jul 30 Aug 19 Sep 1 Oct 6 a a> Integrated I •o r nn^nn Fl

120C 360C 620C 840C 680C O 25 50 25 50 255 0 0 255 0 0 255 0 0 255 0 0 255 0 0 255 0 Percentage of the total population

Figure3.1: Proportional verticaldistribution, partitioned in occurrencein or between plant rows (sampleunits on intermediate positions discarded),in the upper 0.4m ofthe profile during the growingseason 1986 (crop:winter wheat). Valuesfor the0.1 - 0.25 m and 0.25to 0.4m dividedby 3 for comparability withupper layers. Numbersdenote mean number/m 2 onthe samplingdate.

Betweenrows Inplant rows

Figs.3. 1 and3. 2sho wth eproportiona lvertica ldistributio no fenchytraei dnumber s inth esub-layer so fth e0 - 4 0c mlayer ,partitione di noccurrenc ei no rbetwee nplan t rows,fo rth egrowin gseason so f 1986an d1987 ,respectively . Inth eintegrate dan d minimumtillag efield sth eenchytraeid swer egenerall yconcentrate di nth euppe r1 0 cm

42 Conventional Minimum tillage I rPFF j | 1700C 7700C I1700 C 950C 3600C 8600C 5400C 4200C sz May 2 Jun 30 Sep 1 Oct 27 May 2 Jun 30 Sep 1 Oct 27 Integrated I Integrated II PI m r\¥\

1700C 3400C 6400C 0 25 50 0 25 50 0 25 50 0 25 50 0 25 50 0 25 50 0 25 50 0 25 50 Percentage of the total population Figure 3.2: Proportionalvertical distribution, partitioned in occurrencein orbetween plant rows (sampleunits onintermediate positions discarded),in the upper 0.4m ofthe profile during the growing season 1987(crop: sugar beet). Valuesfor the0.1 • 0.25 m and 0.25to 0.4 m divided by3 for comparability withupper layers. Numbersdenote mean number/nf on thesampling date.

Betweenrows Inplant rows

ofth esoi lprofil e (P< 0.01 , Friedmantest) . Inth econventiona lfiel dsignificantl ymor e animals occurredi nth e1 0- 4 0c mlayer sdurin g198 6( P< 0.05 , Friedmantest) ;durin g 1987n osignifican tdifference swer efoun dbetwee nth evariou s layerso fthi sfield . Aneffec t ofplan t positioni ssee nclearl y inbot hyears :i nth euppe r5 t o 10 cm layersgenerall ymor eanimal swer efoun di nth eplan tro wtha nbetwee nrows . Analy­ siso fvariance ,wit hplan tpositio n andtim ea sfactors ,showe d inmos tcase sa signifi­ cant (P< 0.05 ) effect ofplan tpositio n inthes elayers . InConventiona lth einteractio no f timean dplan tpositio nwa ssignifican t (P< 0.05 ) inth e0 - 5 c mlaye ri n1987 . InInte ­ grated IIn osignifican t effects of plantpositio ncoul d beestablished ,du et olarg evari ­ abilityi n thedata .

43 3.3.3.Th e canonical correspondence analyses

SPECIES!

0 RH KHCIO»

• En±\jtn»* bucWnlzl

A tanlaa pareunia

V tail eo v*itr iou iOK I

j^PUW O Bücttwlzla oppondlouloto

o Frldorlcla bulboldm

o Frldvlcla «p. R

D Frldirlcla ap. fl

Q Frlofcrlcia ap. C

DEPTH!

• a - S cm

e 5 - 10 en

• 10 - £6 en

• £5 - 40 oi

Figure 3.3:Ordination diagram based oncanonical correspondenceanalysis of Conventional and IntegratedI. 78.9%of the varianceaccounted for. Scaleof environmental variables-0.2 to 0.2; scaleof species -4to 4. Eigenvalueof first axis 0.092, ofsecond axis0.043. Environmental variables(arrows) are: DATE: number ofdays fromthe start ofthe sampling program; RAIN: precipitation ofthe three weekspreceding asampling date; SOIL20:mean soil temperature at 20 cmof the three weekspreceding asampling date; PLDEEP:Conventional (conventional ploughing depth);PLUNDEEP: integrated I (reducedploughing depth).

Fig. 3.3present sth eordinatio ndiagra mfo rth e firsttw oaxe si nth eanalysi so f the abundancedat ao fbot hyear so fdetaile dsamplin gfo rConventiona lan dIntegrate dI (accountingfo r78.9 % ofth evariance ) andfig . 3.4th ediagra mfro mth efirs ttw oaxe si n theanalysi so f1987 ,fo ral lfield s (accountingfo r69.9 % ofth evariance) . Inthes e diagrams,projectio no fth ehea do fa narro wo na naxi sindicate sth erelativ eimpor ­ tanceo fa facto rfo rtha taxis ,an dprojectio no fth especie s pointso na narro windicate s therespons eo fth eenchytraeid st otha tfactor . Forexample :i nFigur e3. 3th earro wfo r "DATE"(i.e .no .o fday spas tsinc eth estar to fth esamplin g programme) runssouth -• east. Thus,fo ra particula r soillayer ,a specie soccur s mostfrequentl yearl yi n the sampling programmei fit ssymbo llie si nth e North-Westpar to fth ediagram ,an dlate r inth esamplin g programmei fi tlie si nth eSouth-Eas tpart . Themai nfactor sinfluencin genchytraei d abundance,specie scompositio n and verticaldistributio nappea rt o havebee nth etyp eo ffield ,th esoi ltemperatur ean d the

44 Figure 3.4: Ordinationdiagram based oncanonical correspondence analysis ofall sampled fields. 69.9%of the varianceaccounted for. Scaleof environmentalvariables -0.2 to 0.2;scale of species-6 to6. Eigenvalueof firstaxis 0.075, ofsecond axis 0.052. Environmentalvariables (arrows)are: RAIN:precipitation of thethree weeks preceding asampling date; SOIL20: mean soil temperatureat 20 cmof thethree weekspreceding asampling; PLDEEP: Conventional (conventionalploughing depth);PLUNDEEP: IntegratedI and IntegratedII (reducedploughing depth); PLMIN: theintegrated field withminimal tillage; LEY:the field which hadleys inthe formerrotation (IntegratedI); FERT: thefields witha conventional history (Conventional and IntegratedII). factortim e (fig.3.3 ,"DATE") ,an dmuc hles sth eamoun to fprecipitatio n ofth e preced­ ing3 weeks . Thereals ower econsiderabl e interspecific differences inth erespons et oth e factors includedi nth eanalyses . Theconventiona lfiel d(indicate db y"PLDEEP" )wa s characterized bypopulation soccurrin g inth e 10- 4 0c mlayer ,whil e inth eothe rfield s populationswer econcentrate d inth e0 -1 0 cmlayer . Athighe rsoi ltemperature smos t speciestende dt ooccu rnea rth esurface ,a tlowe rtemperature s inth edeepe rlayers , exceptfo rFridericia sp.A andF. sp. C, thatwer efoun dmor eofte n inth e5 -1 0c m layera tlo wtemperatures . Figure3. 3demonstrate s aconsiderabl e changei ntim efo rth eoccurrenc e ofsom e species. Inth ecours eo ftim eFridericia sp. Cwa sfoun dless ,especiall y inth e 10- 40c mlayer ,an dHenlea ventriculosa occurredmor eofte n inth e1 0- 4 0c mlayer . Buchholzia appendiculata occurred lessi nth e5 -1 0 cmlaye r in thecours eo fth e

45 sample programme. Figure 3.4 shows that thefield s with a conventional history (Conventional and Integrated II,indicate d by "FERT") may be characterized by F. bulboides andB. ap- pendiculata occurring morefrequentl y in the 10- 4 0 cm layer and F.sp. A in the 0-1 0 cm layer. The integrated fields, designated with "PLUNDEEP", were character­ ized byth e morefrequen t occurrence of F bulboides and also by F.sp. A. in the 0 -10 cm layer. The integrated field with minimum tillage ("PLMIN") was distinguished by H. ventriculosa and F. sp. B. inth e upper layer and by the more frequent occurrence of F sp. C.

3.3.4. Relations between body weight and length

The data on length andweigh t of thefreeze-drie d potwormswer e used to calculate regression equations of length on dryweigh t for the species found in the investigated fields. Table 3.3 lists the resulting equations, and the number of specimens used in the calculations. For Marionina sp., which very sporadically occurred,th e equation for Enchytraeus buchholzi was used.

Table3.3.: Regression equationsfor length on dryweight, correlations (R), andnumbers of observations(N) forenchytraeid species found at the Lovinkhoeve experimental site. W= dry weightin ng; L= length inmm.

Species Equation R N

Enchytraeus buchholzi W=0.924*L1977 0.904 567 Henlea perpusilla W=0.810*L2068 0.915 213 Henlea ventriculosa W=0.425*L2620 0.956 36 Buchholzia appendiculata W=1.341*L1776 0.907 38 Fridericia bulboides W=0.856*L19'2 0.956 38 Fridericia sp.A W=1.316*L1677 0.937 129 Fridericia sp.B W=1.528*L,7°3 0.907 196 Fridericia sp.C W=1.668*L1569 0.933 19

3.3.5. Population dynamics

Figures 3.5,3.6 and 3.7 show the dynamics of enchytraeid numbers and biomass inth e upper 40 cm of the soilprofile , and the depth distributions of the populations. For 1985 and 1987th e general picture istha t maxima inabundanc e and biomass occurred in spring/early summer, and minima in latewinter . In 1986,wit h a dry spell inJun e and July, low numbers also occurred in summer (Figures 3.5 and 3.6). As regards the

46 Conventional

JIL. JJ 1987 1988

Integrated

w ONDJ F M A MJ J ASONDJ F MA M J J ASONDJ FM Figure3.5: Mean abundance (numbers/nt), partitioned in various layers, fromMay 1985to April 1988in Conventional and Integrated I.

0-5cm 5-10cm

10-25cm 25-40 cm

Conventional

J_d L-IL^JLI 1985 1986 1987 1988

Integrated

Figure3.6: Mean biomass (g dw/nf), partitionedin various layers, fromMay 1985to April 1988 in Conventionaland Integrated I.

0-5cm 5-10cm

10-25cm 25-40 cm

47 Integrated II J 75 (O •o c (O 60 Cfl 3 O £ 25 • IUI 1987 1988

î 1.0 •o

Bill I I AMJ J AéÓNófFMX F/ijwe3.7 :Wea nabundance (number^m2)andbiomass (gdw/nf),partitioned in various layers, fromMay 1987to April 1988 in Integrated II and Minimum tillage.

0-5cm 5-10cm

'»"^ 10-25cm 25-40 cm sampledprofil ea sa whole ,larges tnumber san dbiomas swer efoun di nth eminimu m tillagefiel d (P< 0.05 , Kruskall-Wallistest) ,whil eth eothe rthre efield sgenerall y showedn osignifican tdifference s inabundanc eo rbiomass . Aclea rexceptio nt othi s occurredi nth econventiona lfield ,wher enumber san dbiomas swer esharpl ydecline d inOctobe r 1986,thre eweek safte rth esoi li nthi sfiel dha dbee nfumigate d(1,3-dichlo - ropropene,15 0 l/ha). Numbersan dbiomas si nth econventiona lfiel dwer egenerall ydistribute ddeepe r thani nth eothe rthre efields ,wher epopulation swer emor econcentrate d inth euppe r layers. Thiswa scorroborate d byanalyse so fvarianc eo fth edat awit htime ,soi ltem ­ peraturea t2 0c man dprecipitatio no fth eprecedin g3 week sa s(»variables . These analysesshowe da significan teffec t (P< 0.05 ) ofth efiel dfo rth euppe r5 t o1 0c man d forth e2 5- 4 0c mlayer san dhighl ysignifican t (P< 0.001 )effect s ofth e interactiono f fieldan ddepth . Theminimu mtillag efiel dconstitute da nexceptio nt othis ;o nsevera l occasions largepopulation s notonl yoccurre di nth euppe rlayers ,bu tals oi nth e 10- 40c mlayer s ofthi sfield .

48 3.3.6. Respiration and production

Table3. 4list smea nabundanc ean dbiomass ,an dcalculate drespiratio nan d consumption ing C/m 2fo r 1985t o198 7a tvariou sdepth s inth eprofile . Inth e conven­ tionalfiel dnumbers ,an deve nmor ebiomass ,respiratio nan dconsumption ,wer econ ­ centrated inth e1 0- 4 0c mlayer ,indicatin g morean dlarge ranimal si nthes e layersa s comparedwit hth e0 -1 0 cmlayers . Thisphenomeno nwa smos textrem ei nth e(rela ­ tivelydry )yea r 1986. Inintegrate d I thesituatio nappear st ohav ebee nmor ecomplex : in198 5b yfa rth elarge r parto fth epopulatio nwa sfoun di nth e1 0- 4 0c mlayers . In 1986th eproportio no fth epopulatio n inth e0 -1 0 cmlaye rwa s increased relativet o 1985an di n198 7th egreate r parto fth epopulatio noccurre di nthes euppe rlayers , showinga distributio ntha tconcurre dwit hth eothe rtw ointegrate dfield si nthi syear .

Table3.4: Mean abundance (A)in numbers/m 2and biomass (B) in g C/rrfand estimates of respiration(R) and consumption (C)as g C/rrf/yrin threeconsecutive years.

1985 1986 1987 Field Depth A B R C A B R C A B R C

Conventional 0 -5 cm 3465 0.013 0.285 1.699 1465 0.007 0.098 0.582 3538 0.013 0.348 2.073 5-10 cm 1507 0.010 0.176 1.049 985 0.007 0.090 0.537 5489 0.035 0.765 4.551 10-25 cm 7045 0.080 1.283 7.636 6552 0.064 0.687 4.089 9068 0.073 1.422 8.467 '25 - 40 cm 5810 0.170 0.961 5.718 4388 0.040 0.549 3.268 5750 0.061 1.080 6.428 0-40 cm 17827 0.273 2.705 16.102 13390 0.118 1.424 8.476 23845 0.182 3.615 21.519

Integrated I 0-5cm 3130 0.015 0.343 7.040 2382 0.008 0.170 1.013 10618 0.112 1.843 10.968 5 -10 cm 1804 0.011 0.213 1.270 1792 0.009 0.153 0.912 3922 0.024 0.493 2.936 10-25 cm 9327 0.076 1.290 7.681 4112 0.038 0.452 2.689 8474 0.070 1.311 7.802 25-40 cm 7810 0.180 1.305 7.769 2565 0.025 0.307 1.829 2558 0.034 0.524 3.117 0-40 cm 22071 0.282 3.151 18.760 10851 0.080 1.082 6.443 25572 0.240 4.171 24.823

Integrated II 0-5cm 12054 0.096 2.038 12.130 5-10cm 6392 0.056 1.157 6.888 10-25 cm 6812 0.074 1.324 7.880 25-40 cm 2016 0.030 0.433 2.580 0-40 cm 27274 0.256 4.952 29.478

Minimum 0-5cm 16477 0.131 2.733 16.268 tillage 5-10 cm 6890 0.050 1.049 6.247 / 10-25 cm 11233 0.128 2.222 13.225 25-40 cm 8407 0.113 1.819 10.829 0-40 cm 43007 0.422 7.823 46.569

Comparedwit hth eyear s198 5an d1987,198 6seem st ohav ebee na nextrem e year,wher eth eenchytraei dpopulatio nwa sno tmuc hdevelope dan dconsequentl y respiration andconsumptio nwer elow . Inthi sextrem eyea rth epopulatio nwa sbette r developed inth econventiona lfiel dtha ni nIntegrate dI , whilei nbot hothe ryear sth e reversewa sth ecase . Theestimate so f respirationan dconsumptio n (Table3.4 )wer elowes tfo rinte ­ grated Ii n198 6(1.0 8an d6.4 4g C/m 2) andhighes ti nMinimu mtillag ei n 1987(7.8 2

49 and46.5 7g C/m 2). Thiscorrespond swit h0.52 %t o3.73 %o fth eorgani ccarbo ninpu t (tromorgani cfertilize r andcro presidues ) respired,an d3.07 %t o22.18 %o fi tcon ­ sumedb yth eenchytraeid s inth eintegrate dfields . Inth econventiona lfiel dthes e rangeswer e 1.02%t o2.58 %an d6.05 %t o15.37 %respectively .

3.3.7. Nitrogen turnover

InFigure s3. 8an d3. 9th ecalculate dnitroge nturnove rfo rbimonthl yperiod si s shownfo rConventiona lan dIntegrate dI . Thesefigure s indicatetha tther ewa sa n appreciablenitroge nflu xfro mth eenchytraei d populations,wit hth eexceptio no fth e February/March periodi n198 7an d1988 ,whe nnitroge nwa saccumulate d inth e popu­ lations. Aswit hnumbers ,biomas san drespiration ,mos to fth eflu xoccurre di nth e superficial (0-1 0 cm)layer s inintegrate d I from 1986onwards ,an di nth edeepe r (10-40 cm) layers inth econventiona lfield .

100 - £ 0) ü (0 O a (0 O +-< c o E c - 200 0 CM £ - 100 E Z Z ö) £ E -50 JJASONDJFMAMJJASONDJFMAMJJASONDJFM 1985 1986 1987 1988 Figure3.8: Estimated nitrogen turnover in enchytraeid tissue in Conventional. Barsdenote bimonthlynitrogen turnover in various layers. Theline denotes monthly nitrogen turnover the in completesampled depth.

0-5cm 5-10cm

f h\ 10-25cm 25-40cm

50 100 £ o <0 50 O

a I M Jfc plrtTT^. r6L (O 0 W* o .c 6 c E -50 200 O (M CM E 100 Z Ol £

JJASONDJFMAMJJASONDJFMAMJJASONDJFM -50 1985 1986 1987 1988 Figure 3.9:Estimated nitrogen turnover in enchytraeid tissue in Integrated I. Bars denote bimonthly nitrogen turnoverin various layers. Theline denotes monthly nitrogen turnoverin the complete sampleddepth.

0-5cm 5-10cm

10-25cm 25- 40 cm

Maximum nitrogen flux in the sampled profile occurred in1987 , inIntegrate d I in the period June-November with atleas t 0.13 mg N/m2/month and inConventiona li n June-September with 0.16 mg N/m2/month. Total N-fluxfrom the enchytraeid popula­ tions in198 7amounte d to0.5 3 g/m2fo r the conventional field (fig.3.8 ) and 0.60 g/m2 for Integrated I (fig. 3.9). In 1986 nitrogen flux was low as compared with 1985 and 1987, inIntegrate d Iwit h a rather constant level ofc a 0.02 gN/m 2/month anda tota lflu x of0.1 9 g/m2, inConven ­ tional more variable, with amaximu m of0.0 6 g N/m2/month inMa y and aminimu mo f 0.004g N/m2/month inJuly , the totalflu x amounting to 0.27 g/m2. In Integrated IIan d Minimum tillage,th e general picture in 1987wa s the samea s in Conventional and Integrated I, maxima occurring inMinimu m tillage inth e period July-September with 0.26 gN/m 2/month and inIntegrate d IIi nth e period August-Octo­ berwit h 0.17g N/m2/month.

51 3.4.Discussio n

Thedat ao npopulatio ndynamic san dproductio nobtaine di nth epresen tstud yar e inth esam eorde ro fmagnitud ea sthos ereporte di na numbe ro fothe rstudie so n Enchytraeidae inarabl efield s (Ryl, 1977,1980;Lagerlöf ,1987 ;Lagerlö f etal. ,1989) . Remarkablehowever ,i sth efac tthat ,thoug hmea nabundance so fenchytraeid sar e generallyappreciabl y higher inth epresen tstudy ,biomas sestimate sar emor eclos et o thevalue sobtaine di nthes estudies . Partlythi sma yb edu et omethodologica ldiffer ­ encesi nth eapproac ht oestimat estandin gcrop ,partl ywit hrea lpopulatio ncharacteris ­ tics. Abrahamsen(1973 ) presents regression equationso flengt ho nvolum efo ra numbero f enchytraeidspecie sgroups . Assuminga specifi cdensit yo f 1.05 g/cm3 and afres hweight/dr yweigh trati oo f5.5 6(Edwards ,1967 )t o7.6 9 (Ryl,1977 )thes e equa­ tionsca nb ecompare dwit hth eone sobtaine di nth epresen tstudy . Forcorrespondin g species (Enchytraeusbuchholzi, Buchholzia appendiculata, Fridericia bulboides and Henleaperpusilla) therei sgoo dagreement ,althoug hfo rth eLovinkhoev epotworm sth e estimatedweight sten dt ob ehighe rfo rsmalle rsiz eclasse san dlowe rfo r largersiz e classesa scompare dwit hth eanimal sstudie d byAbrahamse n (1973). H. ventriculosa andF. sp.B woul dbelon gt oAbrahamsen' sgrou p F,F. sp. A andF. sp.C t ogrou pE . Ryl's(1977,1980 ) datawer eobtaine dthroug hweighin go fenchytraeid s preserved inalcohol . Therang ei naverag edr yweight spe rindividua lfoun di nthi swa ywa s 12.48- 36.9 2ju g(assumin gth efres hweight/dr yweigh trati ot ob e7.69) . Inth epresen t studyaverag edr yweight s perindividua lrange dfro m12.7 1n g (inIntegrate d Ii n1986 ) to23.5 3n g (theconventiona lfiel di n1987) . Thisma yindicat ea rea ldifferenc ei n meanindividua lsiz eo rspecie scompositio nwit hth eanimal sfoun di nth e Polishstudy . Lagerlöf etal . (1989)o nth eothe r hand,use destimate sfro m Persson& Lohm (1977),assumin g adr yweigh to f5.9 4ja g foranimal s< 2 mm ,41.9 4ju g foranimal so f 2- 6 m man d14 4ju g foranimal s> 6 mm . Application ofth eregressio n equationsfo r theLovinkhoev e potworms resultsi nth econsiderabl ylowe rdr yweight so f1.1,16. 3 and129. 6ju g forth esam eclasses ,whic hi si ngoo dagreemen twit hth efinding so f Abrahamsen (1973),althoug hbot hweigh tdetermination swer eobtaine dvi adifferen t methods.

Mosto fth especies-relate d differencestha twer efoun di nth estatistica lan d nu­ mericalanalyse s inth epresen tstudy ,ca nno tsatisfactoril y beexplained ,becaus eo f thelac ko f specificecologica l knowledgeabou tth eEnchytraeidae . Theoccurrenc eo f thesedifferences ,however , mayserv ea sa nindicatio no fappreciabl eecologica lvari ­ ationwithi nthi sfamily ,an dstresse sth enee dfo r research inthi sfield .

52 Thepresen tmanagemen tfo rth einvestigate dfield sa tth eLovinkhoev eexperi ­ mentalsit estarte donl yshortl ybefor eth estar to fth esamplin g programme;thu si ti s reasonablet oexpec ttha tth esoi lcommunitie swer eno tye tadapte dt oth emanage ­ ment. Thehistor yan dsuccessiona lstag eo fth efield sma yhav eplaye da nimportan t part. Thisi sreflecte d inth esignifican t increasei nspecie sdiversit yi nIntegrate d I as opposedt oth econventiona lfield ,wher etyp eo fmanagemen twa schange dt oa muc h lesserdegree . Again, thelarg epopulation sfoun di nth edeepe rlayer so fth eminimu m tillagefiel dma yreflec tth einfluenc eo fth eforme rmanagement . Asth eeffect so fth etransitio nan do fth epreviou smanagemen ttype swil lstil lhav e playeda nimportan trole ,th epresen ttreatment sca nno teasil yb eevaluate da tthi s stage. Moreover,a si nth eLovinkhoev e Programmeonl yneste dreplicate sar epresent , iti sno tpossibl et oestablis ha statisticall ysignifican teffec to fth edifferen t agricultural regimes. Yet,ther ear esom eindication so fsuc heffects . Thesudde ndro po f enchytraeid numbersan dbiomas si nth econventiona lfiel dafte rfumigatio nwit hth e nematicide1,3-dichloropropen ei nseptembe r1986 , wasno tparallelle d inIntegrate dI , wheren osuc hfumigatio ntoo kplace . Thisallege deffec to fth efumigatio n probably lastedn olonge rtha ntw omonths . Alonge r lasting influenceo fth eagricultura lpractic ema yoriginat efro mdiffer ­ encesi ntillage . Bothi nth eanalyse so fvarianc ean di nth ecanonica lcorrespondenc e analysesth econventiona lan dintegrate dfield swer echaracterize d bydifference si n depthdistributio no fth eenchytraeids . Inth econventiona lfiel da larg epar to fth e popu­ lation(o naverag e72 %throughou tth eyear )wa sfoun di nth e1 0- 4 0c mlayer . Atthi s depthfres horgani cmateria li sburie dwit hploughing . Inthi s respect,th ecours eo fth e enchytraeidpopulatio ni nIntegrate dI ,whic hha dconventiona ltillag etil lautum n1985 , isillustrative . In1985 ,o naverag e78 %o fth epopulatio nwa sfoun di nth e1 0- 4 0 cm layeri nthi sfield . In198 6an d1987 ,whe nploughin gwa sonl yt o1 5cm ,62 %an d 43% respectivelywa sfoun di nthi s layer. Again, theintegrate dfiel dwit hminimu mtillage , whichwa sconventionall y managedtil lautum n 1986,stil lshowe dhig hnumber san d biomassi nth e1 0- 4 0c mlayer si n1987 . Thesefinding scorrespon dwit hdat afro m Poland (Ryl,1977,1980) ,German y(Zimmermann ,1987 )an dSwede n (Lagerlöfe tal. , 1989),wher eploughin g resultedi na neven ,vertica ldistribution ,o reve na concentra ­ tioni ndeepe rlayer so fth eenchytraei dpopulations . Thesedat aclearl ysugges ta nassociatio no fenchytraeid swit hfres horgani c material,whethe rdirectl ya ssaprovore s (Latter, 1977)o rindirectl ya smicrobivore s (Toutaine tal. , 1982). Thelarge r numberso fenchytraeid s inth eplan trows ,als o re­ portedb yWa y& Scope s (1968),poin tt oa nassociatio nwit hdecayin g roots,wit hroo t exudates,o rt omor efavourabl eabioti ccondition snea rth eplant .

Seasonaldynamic so fnumber san dbiomas sdi dno tdiffe r muchbetwee nth e investigatedfields . Therewas ,however ,a notabl edifferenc e betweenyears :198 6 on theon ehan dan d198 5an d198 7o nth eother . In198 6a summe r minimumoccurred ,

53 andmea nabundanc ean dbiomas si nthi syea rwer elo wa scompare dwit h 1985 and 1987. Asthi ssumme rminimu mcoincide dwit hth edr yspel li nsumme r 1986,a causa l relation mayb epresumed , whetherdirectl ythroug hadvers eeffect so fdrough to n enchytraeids,o rindirectl ythroug ha reduce dactivit yo fth esoi lmicroflora . Ina numbe r ofothe rstudies ,e.g .Nielsen ,1955b ;Möller ,1967 ;Gröngröft , 1981; Hotanen, 1986, moisturewa sidentifie da sa ke yfacto ri nth epopulatio ndynamic so f Enchytraeidae. Moreover,th econventiona lfiel dshowe dhighe rnumber san drespiratio ntha nInte ­ gratedI i n1986 ,an da greate rpar to fth epopulatio n inthi sfiel dwa salway sfoun di n the1 0• 4 0c mlayers ,tha tar eles ssusceptibl et odrought . Yet,fro mth ecanonica l correspondence analysisfo rConventiona lan dIntegrate d Ii nth eperio d 1986t o1988 ,i t appearstha tprecipitatio nwa so fmino rimportanc ea sa nexplanator yfacto rfo rth e populationdynamic s inou rfields ,an dtha tth eenchytraei dpopulation swer emuc h moreinfluence d byth etyp eo ffiel dan dth ecours eo fsoi ltemperature . Althoughth e amounto fprecipitatio n doespla ya rol eo nth ethir dan dfourt h environmentalaxi si n thisanalysis ,tha texplai nth eremainde ro fth evariance ,thes eresult sindicat etha tsoi l moisturea ssuc hma yno thav ebee na ke yfacto r inth epresen tstudy . Moisturecondi ­ tions maylargel yinfluenc eenchytraei dpopulation sthroug hothe rfactors ,lik etempera ­ ture. Clearly, moreresearc h isneede dt oaddres sthi spoin tsatisfactorily .

Anotherfacto rtha tma yhav eplaye da par ti nth edifference s betweensampl e years,i sth etyp eo fcro pgrow nan dth eassociate ddifference s inmanagemen tprac ­ tices. Differenttype so fcro pma yinfluenc eenchytraei d populationsthroug hqualitativ e andquantitativ edifference s inorgani cmateria lenterin gth esoi lsystem ,an dthroug h microclimatologicaleffects . Ryl(1977,1980 )suggeste dtha troo tcrops ,lik epotatoe s andsuga rbeet ,ar emor esuitabl etha ncereal sfo rth edevelopmen to fenchytraei d populations. Frommor enatura lhabitat sther eals oar eindication stha tth etyp eo f vegetationma yinfluenc eenchytraei d populations (amongothers :Abrahamsen ,1972 ; Standen,1980b) .

Therespons eo fth eenchytraeid st olo wtemperatures ,a si ssee ni nth ecanonica l correspondenceanalyses ,i sanothe raspec to fth eseasona ldynamics . Fromthes e analysesi tseem slikel ytha tth eenchytraeid stha tsurviv eth ewinte r perioda sjuvenile s oradults ,d othi s inth edeepe rlayers . Exceptionsar eFridericia sp. A andF. sp.C, that seemt osurviv emainl yi nth e5 -1 0 cmlayer . Invie wo fth erapi dincreas e innumber s inspring ,a substantia lpar to fth epopulation s mayhibernat ea scocoons ,o rth erepro ­ ductivepotentia lo fhibernate dpopulation s mayb ever yhigh . Agriculturalmeasure s however,notabl yploughin gan dth eus eo f pesticides,wil l haveha da nadditiona linfluenc eo nth eseasona ldynamics , whichi sreflecte dmainl yi n theconventiona lfield ,wher enumber sdroppe dt oalmos tcompletel yzer oleve lafte r soilfumigation ,an dten dt ob ever yhig hi nth e1 0- 2 5c mlaye rafte rploughing .

54 Themetho duse dt ocalculat eproductio nbiologica lparameter si smor ecompli ­ catedtha nth eone spropose db yStande n(1980a )an dMoor e& D eRuite r (inpress) , thatar ebase do nth eus eo faverag ebiomass . Yet,th eforme rmetho dwa schose n because itallow sfo rseasona lvariabilit y inintensit yo fpopulatio nmetabolism . More­ over,result so fth elatte r methodsstrongl ydepen do nestimate so f populationturnover , andto olittl ei sknow nabou tlif ehistories ,an dthei rseasona lvariability ,o f enchytraeids toappl ythi sapproac hfruitfully . Onth eothe rhand ,thes emethod sma yb euse dcon ­ versely,t oobtai na nestimat eo fenchytraei dpopulatio nturnove ran dth erati oo fpro ­ ductiont oaverag ebiomas s (P/Bratio) . Applyingthes emethod st oth epresen tbio ­ massdata ,an dassumin gth esam eecologica lefficiencies ,i twa sfoun dtha tth e popu­ lationturnove ran dP/ Brati omus thav ebee napproximatel y 10o naverag ei nth einves ­ tigatedfields . Appliedt oth eresult so fth eSwedis hstud yo f Lagerlöfe tal . (1989), an estimateo fapproximatel y5 results ,th elowe rvalu ebein ga consequenc eo fth ehighe r individualbiomas si ntha tstudy . Standen(1980a) ,however ,considere d P/B ratioso f 1-4fo rterrestria lenchytraei dpopulation sa splausible . Thesehig hestimate so f P/B mayo nth eon ehan db eexplaine db ystron greproductiv eactivit yo fenchytraei dpopu ­ lationsi narabl efields ,tha tar enotoriousl yunstable . Onth eothe rhand ,th eproductio n efficiency of0.4 ,a spropose db yHea l& MacLea n (1975),ma yb ea noverestimate ,a s inth epresen tand ,t oa lesse rextent ,i nth eSwedis hstudy ,a larg epar to fth epopula ­ tionsconsiste do fsmal lworms ,whic hmigh tmea nrelativel yhig hrespirator y costsan d alowe r productionefficiency . Forearthworms ,Le e(1985 ) mentioned aP/ B ratioo f2 to 7,whic hsuggest stha tth epresen testimate s mayafte ral lno tb eunrealistic . Thepresen testimate so fproductio necologica lparameter sare ,du et oa greate r sampling depthan dlarge rnumber si ncombinatio nwit hlowe rindividua lweights ,gener ­ allyhighe rtha nthos efoun di nothe rstudie si narabl efield s(Kasprzak ,1982 ;Lagerlö f etal. , 1989),bu tsta yi nth esam eorde ro fmagnitude . Paustiane tal . (1990)reporte d fromSwedis harabl efield sa proportio no f3. 5- 23 %o ftota lfauna lrespiratio nattribut ­ ablet opotworms . Theavailabl eevidenc ethu smake si tplausibl etha tEnchytraeida e area nimportan tfauna lgroup ,bot hi nconventiona lan di nintegrate dagricultur ei n temperateregions ,an dtha tth edecompositio n oforgani cmatte ri narabl esystem si s considerablyinfluence db yenchytraei dactivity .

Theestimate so nnitroge nturnove rsuppor tth eide atha tpotworm sconstitut ea n importantpoo lo f nutrients. Inthi srespec ti tmus tb etake nint oconsideratio ntha tth e estimates inthi sstud yonl yconcer nth eamount so f nitrogeni nenchytraei dtissue . Nitrogeni nexcrements ,urine so rmucu swer eneglecte d becauseo f lacko fknowledg e aboutthei r nitrogenconten tan dth eamount sproduced . Indirecteffect s ofenchytraei d activityo nnitroge n mobilization,vi astimulatio no fmicrobia lactivity ,wer eals oignored . Whendat afo rearthworm s (Christensen,1987 )ar etake na sa cue ,th eestimate swoul d atleas t be15 %higher . Abrahamsen(1990 )estimate dtha tth econtributio n ofminera l nitrogenfro mdea dtissu eo fCognettia sphagnetorumwa sonl y40 %o fth enitroge n

55 mobilizedthroug hth eactivit yo fthi senchytraei dspecies . Thusth eactua lcontributio n ofenchytraeid st onitroge nmobilizatio nma yhav ebee nconsiderabl y highertha n the estimatescalculate di nth epresen tstudy . Whatpar to fth enitroge nflo wfro mth e enchytraeidpopulation sconsist so fsolubl enitroge ncompound s(fro mdecomposin g tissuean dexcreta ) andwha tpar ti simmobilize di nmicrobia lo rpredator ytissu ere ­ mainst ob einvestigated . Inbot hsystem smaximu mnitroge nflu xoccurre dtoward sth een do fth egrowin g season,implicatin ga nenhance dchanc eo flos so fnutrients ,a snutrien tuptak eo fmos t cropsi sdiminishe dthen . Thesam ewa snote dfo rearthworm sb yChristense n(1987) , whosuggeste dth eus eo ffas tgrowin gcove rcrop st ocircumven tth eproble mo fnitro ­ genlos si nautumn . Thesam esuggestio nwoul db ei nplac ei nth epresen tcase .

Themai ndifferenc ebetwee nth econventiona lan dintegrate dagricultura lmanage ­ mentsystem sappear st oli ei nth edept ha twhic hth eenchytraei dactivit ywa s concen­ trated,whic hcoincide dwit hth edept ha twhic horgani cmatte rwa sadde dt oth e sys­ tem. Inth eintegrate dfield senchytraei dpopulation swer egenerall yconcentrate d inth e upperlayers ,whic hmigh trende rth eenchytraeid s susceptiblet oadvers etemperatur e andmoistur econditions . In theconventiona lfiel da greate rpar to fth epopulation slive d indeepe rlayers ,mor eo rles sprotecte dfro madvers eclimati cconditions . Conse­ quently,durin gth edrough ti n198 6mor epotworm swer efoun di nth econventiona lfiel d thani nth eintegrate dfield ,wherea s inth eothe ryear sth eopposit ewa sth ecase . On theothe r hand,plan tnutrient smineralize dthroug henchytraei dactivit yma yru na higherris ko fbein glos tthroug h leachingwhe nthi sactivit ytake s placei ndeepe rlay ­ ers,wher ecro proot sar eles sabundant .

56 4. Life-history ofEnchytraeus buchholzi Vejdovsky,187 9(Oligochaeta ) and population development inartificia lsoi l

Abstract

Theresearc hreporte dher econcerne ddeterminatio n oflife-histor yparame ­ terso fEnchytraeus buchholzi, andthei rapplicabilit y underfiel dconditions . Laboratoryexperiment swer ecarrie dout ,i nwhic hdevelopmen ttimes , num­ berso fcocoon san degg sproduced ,an dlongevit ywer edetermine da tvari ­ oustemperatures . Bya simpl esimulatio n model,dat ao nth epopulatio n development undermor enatura lcondition swer ecompare dwit hprediction s basedo nth elaborator ytrials . Thecomparison sshowed ,tha tpopulatio n development underfiel dcondition s mayfal lshor tt oprediction sa sregard s abundance,bu to n theothe r hand,tha tindividua ldevelopmen tcoul db e appreciablyfaste rtha npredicted . Itseem sprobable ,tha tth ediscrepancie s foundar erelate dwit hth ephysiologica lconditio no fth eexperimenta lanimals .

4.1. Introduction

Enchytraeusbuchholzi wa s foundt ob eth emos tabundan tspecie sa tth eLovink - hoeveexperimenta lfar mi nth eNoordoostpolder , theNetherland s(thi sthesis) ,wher e the Dutch Programmeo nSoi lEcolog yo fArabl eFarmin gSystem s iscarrie dout . Knowledgeo fth elife-histor y characteristics ofthi sspecie swa sconsidere dusefu lfo r gaining insighti nth emechanism sgovernin g populationdynamic so fenchytraeids ,an d alsoindispensabl efo rpopulatio nmodelling . Enchytraeusbuchholzi ha sbee nth e subjecto f severallife-histor ystudie s (Trappmann,1952 ;Springett ,1970 ; Learner, 1972). However,considerabl etaxonomi edifficultie s areassociate dwit hth e buchholzi-group (Bouguenec& Giani ,1987) ,whic hmake sth eidentit yo fth especie s studieduncertain . Moreover,importan tlife-histor y characteristics,suc ha slongevit y andlengt ho fth ereproductiv e period,hav eno tbee ndetermine dyet . Thus,i twa s considered necessaryt ocarr you ta life-histor ystud yo n thespecie sfoun da tth eex ­ perimentalfarm . Toavoi dpossibl econfusio nwit hrelate dspecies ,al lexperiment s werecarrie dou twit hspecimen stha tderive dfro ma singl eindividual .

57 Basedo nthes eexperiment sa mode llo r populationgrowt ho fE. buchholzims developed. Predictionsfro mthi smode lwer ecompare dwit hdat afro mmicrocosm s resemblingth efiel dsituation ,thu senablin ga nevaluatio n ofth elife-histor ycharacteris ­ ticsfoun di nth elaboratory .

4.2.Method s

4.2.1. Life-history characteristics

Experimentswer econducte da t5 differen ttemperatures :4°C ,8°C , 10°C,16° C androo mtemperatur e (18- 20°C) . Thechoic eo fthes etemperature swa sa compro ­ misebetwee nwha twa sconsidere d desirablean davailabl eequipment . Theanimal s werekep ti nsmall ,covere dpetri-dishe s (4c mdiamete r inth e4 an d8° Cseries ,6 cm diameter inth eothe rseries) ,o naga r (1.3%solutio ni nta pwater ) andusin goa tbra na s food. Thedishe swer estore do ntray s inclose drefrigerato r boxeswit ha smal lquantit y ofwate ro nth ebottom ,t oavoi ddesiccation . Eachdis hreceive da fres hcocoo no fEnchytraeus buchholzi, fromstoc kculture s thatoriginate dfro mon esingl especime nfro mth eLovinkhoev eexperimenta lsite . In thisway ,th egenetica lidentit yo fth especimen swa sassured . Inspectiontoo kplac ea t regular intervals,rangin gfro m biweeklya t4" Ct odail ya t1 6an d20"C . Thedishe s weresupplie dwit hquantitie so foa tbra nlarg eenoug ht ob ei nexces sfo rth eworms , andsmal lenoug ht okee pthoroug hinspectio no fth edishe s possible. Ateac hinspec ­ tionth enumbe ro fworm san dth enumbe ro fdeposite dcocoon spe rdis hwer e counted, andcocoon swer eremoved .Th enumbe ro fegg spe rcocoo nwa srecorde d byvisua l examination. Theexperiment s continuedtil lal lth eanimal sha ddied .

Anotherserie so f experimentswa slai dou tt oestablis hth egrowt hrat eo findividu ­ als. Theseexperiment swer econducte da t8 an d16°C ,applyin gth esam emethod sa s above. However,2 cocoon spe rdis hwer eused ,an da tfixe dinterval sth eanimal s from4 dishe swer eremove dan dmeasure dt oth eneares t mm. Thisoccurre djus tafte r hatching,a tth eag eo f 1 week,2 weeks ,4 weeks ,8 week s etc. Inthes eserie sth e numbero fegg spe rcocoo nwa sals orecorded .

58 4.2.2. Population development inartificia l soil cores

Populationdevelopmen t inmor enatura lcircumstance swa sfollowe d insevera l experimentswit h artificialcore s (41 mmdiameter , 25m mheight ) from Lovinkhoeve soil,prepare daccordin gt oth etechniqu edescribe di nchapte r5 . Tothes ecore s5 freshcocoon so fE. buchholziwer eadded . Thecore swer edestructivel ysample di n thecours eo fth eexperiments ,an dth eextracte dworm swer ecounted ,measure dt oth e nearest mm andthei rphenologica lstag erecorded . Oneexperimen twa scarrie dou ti nth elaboratory ,a tWC, withvariou samount so f oatbra n (0,0.5,1 and2 g )adde dt oth esoil . Asecon dlaborator y experimentwa s conducteda t13° Can d15"C ,wit h0. 3g comminute doa tplan tmateria ladded . Datafo ra fiel dsituatio nwer eobtaine dfro mth eexperimen tdescribe d inchapte r6 (thisthesis) ,i nwhic hartificia lcores , with0 o r0. 5g oa tbra nadded ,wer eplace di nsoil .

4.2.3. The model for potential population development

Toobtai na nindicatio no fth eusefulnes s undermor enatura lcircumstance s ofth e life-history characteristicsfoun di nth elaborator yexperiment s onagar ,prediction so f populationdevelopmen t basedo nthes echaracteristic swer ecompare dwit hth eresult s fromth eexperiment swit hartificia lcores . Forthis ,a simple ,temperatur e drivenmode l for potentialpopulatio n development ofE. buchholziwa sconstructed ,base do nth e results ofth elife-histor y experiments (Table4.1 ) andth egrowt hexperiments . The modelignore dth evarianc e inthes edata ,a si twa sprimaril y meantindicative . To simulateth efiel dsituation ,dail ysoi ltemperatur edat aa t1 0c mdept hfro mth eDutc h Meteorological Institutea t DeBil twer e used. Themode lassume da powe rrelatio n betweenth evariou s experimentaltempera ­ turesfo rlengt ho f incubationtim eo fcocoons ,lengt ho fgeneratio n time,longevity ,an d individualgrowth . Equations used were:

I = 319.492T1146 (R=0.973) M = 2399.504*T1498 (R=0.976) L =14048.227T1706 (R=0.994) DL= (120.101*T 0356)/(LEB),wher e

I = lengtho fincubatio ntim eo fcocoon s (days) T = temperature fC) M = lengtho fgeneratio ntim e (days) LE= length(mm ) L = longevity (days) B = 6.938T0254 DL= lengthgrowt h(mm/day )

59 Linearinterpolation s betweendat aa tth evariou sexperimenta ltemperature swer e usedt oobtai nrate so fcocoo nproduction ,percentage so fviabl ecocoon san dpercent ­ ageso fjuvenile ssurvivin gtil lmaturit ya tth evariou stemperatures . Itwa sassume d thatth enumbe ro fyoun ghatchin gfro ma cocoo nwa s2. 5a tal ltemperature sunde r consideration,an dthei r length2 mm. Startingfro ma situation ,i nwhic hnumbe ran dstag eo fworm so rcocoon swer e known,th emode luse ddail ytemperatur edat at ocalculat eth estag eeac hgrou po f animalso rcocoon swoul dhav ereache da tth een do fa day . Cocoonsdeposite do n oneda ywer etreate da sa ne wgroup . Thenumbe ro fworm si nth eartificia lcore san d thephenolog yo fth epopulation swer ecompare dwit hth evalue spredicte db yth e model.

4.3.Result s

4.3.1. Life-history characteristics

Table4. 1sum su pth eresult so fth elife-histor yexperiments ,supplemente dwit h datafro mth eexperiment so ngrowt hrate . Fromthi stabl ei tappear stha tunde rth econdition sstudie dth eoptimu m tempera­ turefo rE. buchholzii si nth erang ebetwee n 10an d20"C ,a sa tthes etemperature sth e percentageso fviabl ecocoon san dth enumbe ro fcocoon sproduce dpe rwor mwer e highest. Therespons et otemperatur ewa smos tmarke da tlowe rtemperatures , where incubationtim ean dgeneratio ntim edecrease dsharpl ywit hrisin gtemperature . Atal ltemperatures ,cocoo n productioncontinue dtil ldeath ,wit hirregula rfluctua ­ tionsi nth ecours eo ftime . However,th enumbe ro fcocoon spe rwor mwa smarkedl y lessa tlowe rtemperatures . Insevera linstance sonl yon ewor mhatche dpe rcocoon . Suchsingl eworm s producednew ,an dviable ,cocoon sa troughl yth esam erat ea sworm stha twer ekep t together,indicatin gth eoccurrenc eo fparthenogenesi s inE. buchholzi.

60 Table4,1: Life-historycharacteristics of E.buchholz iin laboratory experiments. Timegiven in days, n.d.:not determined.

Temperature fC) 4 8 10 16 20

Initial no.o f 50 69 20 37 15 cocoons %viabl e 78.00 88.41 100.00 100.00 93.33

Eggs/viable cocoon 3.44 4.00 2.30 3.41 2.36 Coeff.var . 42.73 33.25 28.70 42.82 39.41 N 39 61 20 37 14 %fertil e 88.66 96.75 93.33 98.24 100.00

Incubation time 56.25 37.46 24.50 11.02 10.55 Coeff. var. 15.98 16.04 11.92 47.46 24.27

Worms/cocoon 3.03 3.87 2.10 3.35 2.36 Coeff. var. 47.52 35.14 21.43 45.07 39.41

No of worms 118 236 42 124 33

Generation time 239.10 145.11 84.57 31.69 25.94 Coeff.var . 35.35 23.11 45.57 27.64 15.15 N 118 280 42 300 33 % surviving till maturity 82.20 94.64 88.10 98.67 93.94

Longevity 640.52 415.14 n.d 112.01 91.70 Coeff. var. 54.18 36.46 n.d 32.37 35.14

Cocoons/worm 15.23 19.75 n.d 53.33 53.09 Coeff. var. 80.30 54.43 n.d 38.14 48.37

Eggs/cocoon 2.41 2.54 2.69 2.51 2.33 Coeff. var. 45.63 42.52 40.15 41.04 36.05 N 700 941 269 3002 88

61 4.3.2.Growt h rates

Thedat afro mth egrowt hrat eexperiment swer euse dt ocalculat eth efollowin g powerregression sdescribin gdail ylengt hgrowth :

at 8'C:G=251.586*L4088 at16°C:G=321.910*L3428,

whereG=proportiona lgrowt h(percentage ) andLHengt h(mm) .

4.3.3. Comparison of model predictions with data from artificial cores

Tables4. 2t o4. 4compar eth epopulatio ndevelopmen tan dphenology ,an dth e sizeo fth eworm s inth eartificia lcore sa scalculate d byth esimulatio n model, withth e valuesobserve d inth elaborator yan d fieldexperiments . Highestnumber so fworm s wereobserve d inth ecore stha t hadorgani cmatte radded . Theobserve d numberso f wormsi nth efiel dexperimen t (Table4.4 ) weregenerall yconsiderabl y lowertha ni n corresponding coresi nth elaborator yexperimen t (Table4.2) . Fromal l3 table si tappear stha tth enumbe ro fworm shatchin gfro mth eorigina l cocoonswer esubstantiall y lowertha nwa spredicte db yth emodel ,th enumber si nth e fieldexperimen t (Table4.4 ) beinglowest . Inth elaborator yexperiment sfewes tjuve ­ nileshatche di nth ecore swit hcomminute doa tplant s (Table4.3) . Deviationsfro m predictedvalue swer ei nmos tcase ssubstantial . Thenumber spredicte db yth emode l weregenerall y(much ) highertha nth eobserve dnumbers ,whic hwa st ob eexpecte d fromth efac ttha tth emode lneglecte dfactor slik efoo davailability ,densit yo fth epopu ­ lationan dnon-natura lmortality . Themos textrem edeviation swer efoun d inth eartifi ­ cialcore swithou tadde dorgani cmaterial . Incore swit horgani cmaterial ,initia lpopula ­ tiongrowt hwa smor eo rles sconcurren twit hth eprediction sfro mth emodel ,i nsom e cases(Tabl e4.2 ) evenconsiderabl y higher. Inth ecours eo ftime ,thes ecore sto ofel l behindth epredicte dvalues . Therewer eals ostron gdeviation s inth ephenolog yo fth epopulation . Inth elabo ­ ratoryexperiment swit hoa tbra nadde d (Table4.2) ,juvenile si nth ecore swit h 1 and 2g oa tbra nadde dreache dhig hdensitie searlie rtha npredicted ,indicatin ga shorte r maturationtim etha nexpecte do ra shorte r incubationtim eo fcocoons . Inth elabora ­ toryexperimen twit hcomminute doa tplan tmateria ladde d(Tabl e4.3) ,adult sappeare d earliertha nexpecte d inth e13° C treatment. Thisphenomeno nwa sno tfoun di nth e 15°Ctreatment . Again,i nth efiel dexperimen t (Table4.4 ) incore swit hoa tbra n added, adultsappeare dcirc a10 0day searlie rtha npredicted . Withn ooa tbra nadded ,bot hi n

62 Table4.2: Comparisonof population size and population phenology aspredicted by themodel with datafrom artificial cores at16°C inthe laboratory, withand withoutoat bran added.

Predicted Observed oatbran : 0 g 0.5g 1 g 2g Days Number Length Number Length Number Length Number Length Number Length

Juvenile;

37 13 5.3 5.80 2.48 3.25 2.38 n.d n.d n.d n.d (±3.03) (±0.69) (±2.63) (±1.12) 43 0 16.00 2.69 n.d n.d 179.50 2.56 71 2.35 (±5.66) (±0.97) (±16.26) (±0.58) (±0.48) 86 533 4.2 33.00 1.83 n.d n.d 303.00 2.87 236 3.64 (±38.18) (±0.71) (±22.63) (±1.04) (±1.22) 91 630 3.9 18.50 2.43 86.60 3.50 n.d n.d n.d n.d (±6.40) (±0.66) (±29.23) (±0.94)

Adults

37 0 . 0 . 6.50 6.92 n.d n.d n.d n.d (±1.29) (±0.39) 43 12 5.6 0.50 5 n.d n.d 17.50 5.71 6 5.17 (±0.71) (±3.54) (±0.46) (±0.41) 86 213 5.7 0 n.d n.d 80 4.38 100 5.20 (±28.28) (±0.49) (±0.40)

91 315 5.8 0 • 0 • n.d n.d n.d n.d

Totals

37 13 5.3 5.80 2.48 9.75 5.41 n.d n.d n.d n.d (±3.03) (±0.69) (±2.50) (±2.28) 43 12 5.6 16.50 2.76 n.d n.d 197.00 2.84 77 2.57 (±4.95) (±1.03) (±19.80) (±1.06) (±0.89) 86 746 4.6 33 1.83 n.d n.d 383 3.18 336 4.11 (±38.18) (±0.71) (±50.91) (±1.13) (±1.27) 91 945 4.5 18.50 2.43 86.60 3.50 n.d n.d n.d n.d (±6.40) (±0.66) (±29.23) (±0.94) thelaborator yan di nth efiel dexperiment ,almos tn omatur eworm swer erecorded . Yet,i nth ecore swithou torgani cmatte radde d(Tabl e4.2) , numberso fjuvenile sha d substantially riseno nth esecon dsampl edate ,pointin gt oa nearl ymaturatio ni nthes e corestoo . Theobserve dpercentage so fjuvenile swer egenerall yhighe rtha npre ­ dicted,excep ti nth ecase swit hearl yappearanc eo fadults . Duet oth edeviation sfro mth eprediction sa sregard sth ephenolog yo fth epopula ­ tionsi nth eexperiments ,siz eo fth eworm sa sobserve dma yonl yb ecompare di nth e earlystage so f populationdevelopment ,befor enewl ylai dcocoon shatched . Incore s withoutorgani c matteradded ,th esiz eo fth eworm swa susuall y lesstha nth epredic ­ tionso fth emode lfo rthes estages ,whil ei ncore swit hadde dorgani cmateria lth e wormsgre waccordin gt oth epredictions .

63 Table 4.3: Comparisonof population sizeand population phenology aspredicted by themodel with datafrom artificial cores at 13and 15'Cin thelaboratory, with0.3 g comminuted oat plant materialadded.

Predicted Observed 13*C 15"C 13'C 15'C Days Number Length Number Length Number Length Number Length

Juveniles

14 0 - 13 2.6 1.00 2.00 1.00 2.00 (±1.73) (±0.00) (±1.00) (±0.00) 42 12 4.9 0 ' 0.40 5.00 2.75 3.27 (±0.55) (±0.00) (±2.50) (±1.85) 84 205 3.6 505 4.2 21.40 3.86 91.33 3.00 (±28.94) (±1.56) (±81.47) (±1.11) 111 425 4.3 2673 3.3 4.20 4.33 12.20 2.90 (±4.08) (±1.93) (±18.12) (±1.40)

Adults

14

42 0 • 12 5.3 0.80 4.75 4.50 4.89 (±1.79) (±0.50) (±2.38) (±0.96) 84 12 6.3 12 6.8 1.40 7.57 6.17 5.24 (±2.61) (±0.53) (±4.67) (±0.72) 111 100 5.6 476 5.9 0.20 7.50 0.30 6.33 (±0.63) (±2.12) (±0.95) (±2.52)

Totals

14 0 - 13 2.6 1.00 2.00 1.00 2.00 (±1.73) (±0.00) (±1.00) (±0.00) 42 12 4.9 12 5.3 1.20 4.83 7.25 4.28 (±1.64) (±0.41) (±4.72) (±1.56) 84 217 3.7 517 4.3 22.8 4.09 97.50 3.14 (±31.51) (±1.76) (±80.88) (±1.21) 111 525 4.5 3149 3.7 4.40 4.48 12.50 2.98 (±4.58) (±2.03) (±18.95) (±1.52)

64 Table 4.4: Comparison ofpopulation size and population phenology aspredicted by themodel with datafrom artificial cores placed in thefield, with and without oat bran added.

Predicted Observed oat bran: 0g 0.5g Days Number Length Number Length Number Length

Juveniles

62 10 3.6 2.06 2.00 0.38 3.17 (±1.98) (±0.00) (±1.09) (±2.14) 98 10 4.1 0.19 1.67 0.94 2.53 (±0.40) (±0.58) (±2.24) (±1.36) 121 10 4.4 1.38 1.68 1.38 1.91 (±1.63) (±0.48) (±1.82) (±1.02) 155 0 0.44 2.00 6.88 2.37 (±0.89) (±0.82) (±8.41) (±1.10) 185 105 3.2 1.44 1.74 45.44 2.44 (±1.46) (±1.10) (±36.32) (±1.04) 216 377 4.2 1.13 2.83 36.69 2.56 (±1.71) (±1.38) (±48.83) (±1.01) 246 8690 3.8 0.38 3.17 3.81 2.83 (±0.83) (±0.94) (±7.38) (±0.86)

Adults

62 0 . 0 . 0.19 5.00 (±0.54) (±1.00) 98 0 0 0.50 6.13 (±0.73) (±2.10) 121 0 0 0.38 5.67 (±0.62) (±2.88) 155 10 5.2 0 2.63 5.33 (±3.63) (±1.16) 185 10 6.1 0.19 5.33 6.50 5.04 (±0.75) (±1.53) (±7.20) (±1.09) 216 138 5.7 0 1.13 3.89 (±1.89) (±1.37) 246 662 6.1 0 - 0

Totals

62 10 3.6 2.06 2.00 0.56 3.78 (±1.98) (±0.00) (±1.36) (±1.99) 98 10 4.1 0.19 1.67 1.44 3.78 (±0.40) (±0.58) (±2.73) (±2.37) 121 10 4.4 1.38 1.68 1.75 2.71 (±1.63) (±0.48) (±2.08) (±2.19) 155 10 5.2 0.44 2.00 9,50 3.19 (±0.89) (±0.82) (±11,25) (±1.73) 185 115 3.4 1.63 2.15 51.94 2.76 (±1.93) (±1.62) (±41.17) (±1.35) 216 515 4.6 1.13 2.83 37.81 2.60 (±1,71) (±1.38) (±48.90) (±1.05) 246 9352 4.0 0.38 3.17 3.81 2.83 (±0.83) (±0.94) (±7,38) (±0.86)

65 4.4.Discussio n

4.4.1. Comparison of the present data with other life-history studies

InTabl e4. 5 literaturedat ao nth elife-histor yo fEnchytraeus buchholzi i nlabora ­ toryexperiment s arecompare dwit hth edat aobtaine di nth epresen tstudy . Asregard s thelengt ho fth eincubatio nperiod ,ther eseem st ob egoo dagreement . Theothe r parameters revealdiscrepancie s betweenth evariou sauthors . Thegeneratio ntime s recordedb yTrappman n (1952)ar eshortest ,followe d bythos efro m Learner (1972),th e presentstud yan dSpringet t (1970) respectively. Therevers eorde r isfoun di nth e numbero fegg spe rcocoon ,Springet t (1970)reportin glowes tnumbers ,Trappman n (1952)th ehighest . Thenumbe ro fobservation s oncocoo nproductio n issomewha t less,bu tpoin tt oappreciabl edifferences ,th evalue si nth epresen tstud ybein ghighes t attemperature s above8°C .

Onewa yo f addressingthes edifference s ist otak eint oconsideratio nth evariou s culturemethod stha twer euse di nth elaborator yexperiments . Trappmann (1952)use d petridishe sline dwit hfilte r paperwhic hwa smoistene dwit hta pwater . Theworm s werefe dwit hoa tbra nan dbread . Learner (1972)use dth esam esetup ,bu ther eth e wormsreceive dactivate dsludg ea sa foo dsource . Springett (1970)culture dth eani ­ malsi npetr idishe swit h 1% soilextrac taga rsprinkle dwit hsoi lan dmoistene dth e mediumwit hdistille d soilsolutio n (Springett, 1964). Asa foo dsourc eleave san dpea t particleswer epresent . Inth epresen tstud ya 1.33 %aga rsolutio ni nta pwate rwa s used,an dth eworm swer efe dwit hoa t bran. Iti sconceivabl etha tth edifference sfoun dma ya tleas tpartl yb edu et oa neffec to f thecultur emediu m(kin do f substratean dth echemica lcompositio no fth ewate rused ) andqualit yan dquantit yo ffood . Filterpape rwoul dserv ebette ra sa mediu mtha n agar,an dbrea d plusoa tbra nmigh tb ea bette rfoo dsourc etha noa tbra nalon eo r activatedsludge . Thelo wnumbe ro fegg spe rcocoo nan dth elon ggeneratio ntim ei n Springett's (1970)culture s mayhav ebee ncause db yshortag eo ffood ,a swa ssug ­ gestedbefor eb yAlber t (1975),o rb yfoo ddeficiencies . Ifth edifference s ingeneratio ntim ean dproductivit ywer ecause db ysuc hexterna l factors,thi swoul dmea ntha tth edevelopmen tan dphenolog yo f populationso f E.buchholzi i nfiel dcondition swil lvar ywidely ,dependin go nth eprevalen tconditions . Anindicatio nfo rsuc hexternall yinduce d responseo fthi sspecie swa sreporte db y Trappmann (1952),wh ofoun dlarg edifference s insiz eo fth eadul tworm s indifferen t feedingconditions ;thi srespons e couldb ereverse do rchange db ychangin gth e amountan dtyp eo ffood .

66 Table 4.5: Someliterature dataon thelife-history of E . buchholzi, fromlaboratory experiments, and results from thepresent study.Upper lines: means, lower lines: ranges (ifdetermined).

'C Incubation period Hatched Generation time Cocoons/adult Eggs/cocoon Author (days) (%) (days) (per week)

4.0 56.3 78.0 239.1 0.27 2.4 this thesis 40-89 180-488 - 0-6 8.0 39.0 76.0 93.0 1.45 3.0 Learner, 1972 35-43 92-93 - 1-9 8.0 37.5 88.4 145.1 0.51 2.5 this thesis 26-61 89-404 0.06-1.36 0-6 10.0 24.5 100.0 84.6 - 2.7 this thesis 15-35 49-194 - 0-5 10.0 35.0 100.0 >180.0 0.63 2.0 Springen, 1970 - - - 2-2 12.0 19.3 98.0 38.3 - 14.9 Trappmann, 1952 14-25 - - 1-44 15.0 11.0 94.0 27.0 1.31 3.0 Learner, 1972 - - - 1-9 16.0 11.0 100.0 31.7 4.65 2.5 this thesis 7-20 26-48 2.59-5.12 0-7 18.0 9.4 94.4 18.4 2.80 14.9 Trappmann, 1952 8-12 - - 1-44 20.0 10.6 93.3 25.9 5.65 2.3 this thesis 6-15 23-36 2.94-6.47 - 20.0 10.0 74.0 25.0 2.62 3.0 Learner, 1972 - - - 1-9 20.0 7.7 100.0 14.7 - 14.9 Trappmann, 1952 6-11 - - 1-44

Asecon dexplanatio nfo rdiscrepancie s betweenth evariou sstudie s mayb efoun d inth etaxonomi eproblem si nth egenu sEnchytraeus, andespeciall y£ buchholzi. This, andrelate dspecies ,presen ta hithert ounsolve dsystemati cproble m(Bouguene c& Giani,1987) . Thus,i ti sconceivabl etha ti nth evariou sstudie s(mixture sof ) different forms oreve ndifferen tspecie swer eused . Intha tcase ,th edifference sfoun dma y reflectspecie s relateddifferences .

4.4.2. Evaluation of the present life-history data

Themode ldevelope dfro mth elaborator ydat ai nth epresen tstud ydescribe s populationdevelopmen t and phenologyunde rth eassumptio ntha tth econdition sfo rth e enchytraeids remainth esame ,viz .a substrat eo fagar ,exces soa tbra na sfood ,ab ­ senceo f predators,parasite san dcompetitors ,an dn oinfluence ,positiv eo rnegative ,

67 frompopulatio ndensity . Itseeme dreasonabl etherefore ,t oexpec ttha tth emode l wouldpredic thighe r populationdensitie san da mor erapi dlif ecycl etha nrecorde di n fieldsituations . Thecompariso nwit hpopulatio ndevelopmen ti nartificia lsoil swhic hwa scarrie d outi nthi sresearc h onlypartl ycorroborate dthes eexpectations . Numberso fanimal s foundi nth eartificia lcore sgenerall ywer elowe rtha npredicte db yth emodel . Initial growtho fth eindividua lworm swa sroughl yaccordin gt oth epredictio ni nth eartificia l soilstha tha dextr afoo dadded ,an dwa sretarde di nth ecore swithou textr afood . At thesam etime ,appreciabl edeviation si nphenologica lcharacteristic swer erecorded , themos timportan tbeing :

- Fromth ecompariso no fpredicte d andobserve dvalue si tappear stha tsurviva lo f E. buchholzii nmor enatura lcondition s isappreciabl y lowertha nfoun di nth e laboratory. Thenumber so fworm stha tsuccessfull y hatchedfro mth eorigina l5 cocoons percor ewer ei nal ltreatment sclearl y lowertha nth evalue sfro mth elife - historyexperiments . Thisma yindicat ea lowe rviabilit yo fcocoon swhe npu ti n soil,o ra muc hmor evariabl eincubatio ntim ei nsoil ,resultin gi na postponemen t ofhatchin gi nth eartificia lcores . - Thepresenc eo rabsenc eo foa tbra ni nth eartificia lcore sappeare dt oinfluenc e life-historycharacteristic s considerably. Bothi nth elaborator yan di nfiel dcondi ­ tionsth eanimal shardl y maturedi ncore swithou toa tbran ,wherea s incore stha t hadoa tbra nadded ,maturatio ntim ewa sshorte rtha npredicted . Inth elaborator y experimentwit hartificia lcore stha tha doa tbra nadded ,tota lnumber sinitiall ywer e muchhighe rtha npredicted ,indicatin gth epresenc eo fa ne wgeneration . Itseem s cleartha ti nthes ecase sbot hhatchin gtim ean dgeneratio ntim efo rth esecond , andpossibl yals olate rgeneration swer eshorte rtha nexpected . Incore swit h comminutedoa tplan tmateria ladded ,thi seffec twa shardl yfound ,indicatin gth e importanceo ffoo dquality . - Theproportio n ofjuvenile s inth eartificia lsoil swa spracticall yalway s highertha n predicted. Thisma ymea ntha teithe rmaturatio nwa spostpone dfo ra n appre­ ciableproportio no fth epopulation ,o rmortalit yi nth ematuratio nperio d(o rdirectl y after maturation) washighe rtha nth evalue sfoun di nth elife-histor yexperiments . Asalmos t nomatur eworm swer erecorde di nth eartificia lsoi lcore swithou toa t branadded ,i twoul dsee mtha tpostponemen to fmaturatio n isth emos tlikel y mechanism.

Evenwhe nth evariabilit y inlife-histor y characteristics (Table4.1) ,whic hwer e ignoredi nth emodel ,i stake nint oaccount ,th edeviation s inobserve d populationphe ­ nologyca nno tb eexplained . Thesefindings ,i ncombinatio nwit hth edat ai nTabl e4.5 , rather indicatetha tth eamoun tan dqualit yo ffoo davailabl eha sha da stron ginfluenc e notonl yo nth epopulatio ndevelopment ,whic hwa st ob eexpected ,bu tals oo nth elife -

68 historycharacteristic s of£ buchholzi.

Toexplai nth edeviation sfro mexpecte dphenology ,severa lhypothese s mayb e suggested: - asoa tbra nwa sth esol efoo dsourc efo rth eenchytraeid si nth elife-histor yexperi ­ ments,i ti sconceivabl etha ta foo ddeficienc ydi dpla ya role ,whic hcause dth e generationtim et ob eprolonged . Inothe rwords ,th eworm sneede dmor etim et o collectenoug ho fcertai nnutritiv esubstance st oreac hmaturity . Inth eartificia l cores,differen tfoo dsubstance swer epresent ,allowin gth eworm st omak eu p for thedeficiencie s inth esupplie dfood . - thephysica lenvironmen t mayb ever yimportan tfo renchytraeids . Agari sno ta verynatura lhabita tfo rthi sspecies ,an dma yimpos edifferen t conditionso n move­ mentan dlocomotio ntha ndoe ssoil . Inth elaborator yculture sth eenchytraeid s oftenwer esee nlyin gagains tth esid eo fth ecultur edish . Thisma yb ebecaus e they needa soli dsubstrat et ofunctio nproperly ,whic hwoul d implya negativ e influenceo fth e(rathe rsoft ) agaro nth erat eo fdevelopmen t ofth eworms . - theearl yoccurrenc eo fadult swa smos tconspicuou s inth efiel dexperimen ti n coreswit hoa tbran . Inthes ecases ,a slightl yacceleratin geffec to ffluctuatin g temperatureso ndevelopmen t (Reynoldson,1943 )ma yhav einvigorate dth eeffec t ofth epresenc eo foa tbra na sfood . - thelo whatchin gsucces so fth eorigina lcocoon s inth eartificia lsoil smigh timpl y thatthes ecocoon swer eno twel ladapte dt oth econdition s insoil . Anyeffec to f themanipulatio no fth ecocoon sca nb eexcluded ,a sth etreatmen to fth ecocoon s wasth esam ea si nth elife-histor y experimentso naga rplates . Perhapsa protec ­ tivelaye raroun dth ecocoo nwa sabsent ,whic hi nth egenu sEnchytraeus, accord­ ingt oChristense n (1956),generall yi sdeposite d byth eadul twor mi nsoil . This couldmea ntha tsom esoi lfactors ,possibl yparasite so rpredators ,adversel y influenced cocoondevelopment . Theprecis enatur eo fthes efactor sremain st ob e elucidated. In viewo fth ever yrapi dpopulatio ndevelopmen twhic hwa srecorde d inth elaborator ycore stha tha doa tbra nadded ,cocoon sdeposite d laterwer e betterprotected .

69 4.4.3. Synthesis

Basedo nth edat apresented ,th efollowin gtentativ econclusion s onth edevelop ­ mento fa n£ buchholzipopulatio n underfiel dcondition sma yb e formulated: - Thepotentia lfo r rapidpopulatio ndevelopmen twhe nsufficien tfoo di savailable ,i n combinationwit hth epossibilit yo f parthenogenetic reproduction,mak e £ buchholzia typica lr-species . Adverseconditions ,lik eshortag eo ffoo dar e mainlysurvive dthroug h prolongationo fth ejuvenil estage ,o reve na retur nt oth e juvenilestage ,a swa sfoun dwit hStercutus niveus (Dózsa-Farkas, 1973c). The adultstag eo fthi sspecies ,and ,possibly ,it scocoon sar eo f minorimportanc ei n thisrespect . Underfavourabl econdition sther ewil lb ea nexponentia lpopulatio n growth,initiate d byaccelerate d maturationo fjuvenile san dhatchin go fcocoons . Underunfavourabl e conditionsth epopulatio nwil lb ereduce dthroug h retardation ofhatchin gan dmaturation ,an dincrease dmortality . - Inth efiel dexperimen twit hartificia lcores ,temperatur ewa svariable ,an dmoistur e wasprobabl yno ta limitin gfactor ,a sdurin gth eexperimen t nodr yspell soccurred . Thus,th eresult s presented hereindicat etha tth eeffec to ftemperatur e onth elife - historywa slargel yoverrule d byth eeffec t offoo davailability . Thiscoul dals ob e anexplanatio nfo rth ecommonl yfoun dautum npea ki npopulatio n densityi n enchytraeids. Probably,population s ofthi sspecie s reactt oth esuppl yo ffres h organic materialan dth eeffec t of lowertemperature s iso fmino rimportance . The sizeo fa natura l populationwil ltherefor eb emainl ycontrolle d byth equalit yan d quantityo ffood . Prédationan dparasitism ,moreover , mayb eo fimportanc ei n determiningth ehatchin g successo fcocoons .

Forothe renchytraei dspecie sthes emechanism s mayno tapply . AsSpringe n (1970)ha sshown ,ther eexis tclea rdifference s betweenvariou sspecie so fpotworm s asregard sappearanc eo fadult san dth ereproductiv e period. In view ofth epropertie s of£ buchholzideduce dhere ,i tma yno tb eexclude dtha tthi sspecie s livedunde r suboptimalcondition s inth efiel dstudie db ySpringet t (1970),whic hresulte d ina pro ­ longedlif ecycle . Thesam ewa sfoun di nth epresen tstud y inth eartificia lcore swith ­ outfoo dadded . Iti shardl yconceivable ,however ,tha tal lspecie sstudie db ySpringet t (1970)experience dsuc hadvers econditions . Itseem smor elikel ytha ta tleas tsom eo f thesespecie sd ohav ea longe r lifecycl ean dhenc eslowe r reactiontha n£ buchholzi.

Thedifference sfoun dbetwee nth eobserve dan dpredicte d populationparameters , andth eexplanation stha t mayb egive nfo rit ,agai nstres stha tcautio n isneede di n applying laboratorydat at ofiel dsituations . Development offiel dpopulation s mayfal l shortt oprediction s basedo nlaborator y data,a si scommonl yobserved ,o r mayexcee d those,a si sshow ni nth epresen tstudy .

70 Anacceleratio no fth elif ecycl eunde rfavourabl econdition sentail sa highe ractiv ­ ityleve lan dfaste r populationgrowt htha npredicte dfro mlaborator yobservations . Underunfavourabl e conditions,th elif ecycl ema yb eprolonged ,an dsiz ean dactivit yo f apopulatio nlowe rtha nexpected . Forproductio n ecologicalcalculation sthi swoul d meantha tdat ao nth ephysiologica lconditio no fa population ,possibl yreflecte d init s phenology,ar eindispensabl efo r makingadequat eestimate so fit sactivity . Itwoul db ehighl yrecommendable ,therefore ,t oestablis hth emai nfactor stha t determineth ephysiologica lconditio no fa species ,an dt ocarr you tlife-histor yexperi ­ mentsvaryin gthes efactor sfro mextremel y unfavourablet oextremel yfavourable . The influenceo fthes efactor so nlife-histor ycharacteristic sshoul dthe nb eintegrate di n modelsfo r populationgrowth .

71 5.A metho dt oconstruc t artificialsoi lcore s fromfiel dsoi lwit ha reproducibl e structure

(with J.C.Y. Marinissen and B. Kroesbergen)

Abstract

Ametho di sdescribe dtha tallow smanipulatio no fsoi lstructur ea sa variabl e inmicrocos mexperiment swhil eleavin gothe r characteristics intact. The basicstep si nth emetho d are: - homogenizationo fth esoi lb ysievin g - partialsterilization ,t oeliminat e largerbiot a - compressiono fa predetermine damoun to fsoi lt oa certai nvolume . Inthi sway ,core sar eproduce dwit hhighl yunifor msoi lphysica lcharacteris ­ tics. Thestructur ema yb eadjuste dt oth eneed so f anexperimen t byvaryin g themes hsiz ei nsievin go rth eamoun to fsoi lt ob ecompressed ,b yintroduc ­ ingartificia lmacropores ,creatin gartificia lbarrier setc . Themetho dha sbee n usedi nexperiment s onth ereaction so fsoi lanimal st ovariou s porestruc ­ tures,studie so nth echange si nsoi lstructur eb ystructur eformin ganimal s andstudie so nroo tgrowth .

5.1. Introduction

Practicaldifficultie s areofte nprohibitiv efo r usingsoi lstructur ea sa variabl ei n microcosmexperiments . Bydefinition ,th estructur eo f undisturbedsoi lcore si s un­ knowna tth eonse to fa n experimentan dlarg eamount so fcore swoul db eneede dt o accountfo rth ehig hspatia lvariabilit y inth efield . Whencla ymineral s (likevermiculit e (VanD eBund ,1972) )o riner tmateria l (likeglas sbeads )ar euse dt oproduc eartificia l structures,th edeviatio nfro mnatura lconditions ,fo r instancei nth ecompositio n ofth e microfloraan dth epresenc eo raccessibilit yo forgani cmaterial ,ma yb eundesirable . Herea metho di spresente dt oproduc eartificia lsoi lcore swit ha highl y reproducible structureusin gfiel dsoil . Themetho dallow sadjustmen to f porosityand , toa lesse r extent,por esiz edistribution .

72 5.2.Descriptio no fth emetho d

Parameterst o beknow n aboutth e soilare :

- specific mass ofth e solid phase - thelowe r plastic limit (Attenberg limit (Burkee tal. , 1986)) ofth e soil, i.e.th e gravi­ metric moisture content below which innorma l agricultural practice occurring pressures can be exertedwit h negligibledeformatio n ofth eaggregates . The cores aret ob eproduce d ata gravimetri c moisture content below this value.

The desired porosity ist ob echose n inadvance . This can betota l porosity or air- filled porosity. The amount ofsoi l (A)neede d can be calculated asfollows :

A=PsV(1-(t>/100)( 1+w/100 )wher e

A=psV(1-(t»g/100)(100+w)/(100+psW) where , isth e air-filled porosity aimedat , and

3 ps=specific mass ofth e soil (kg m' ) V=volume ofth e cores (m3) w=gravimetric water content ofth e soil (% w/w) (Hotal porosity (% v/v)

g=air-filledporosit y (% v/v)

The steps inth e production process are:

Freeze soil fromth efiel d soa st obrea k clods along natural cleavage planes. This step may be skipped ifn oclod s are present. Sieve the soilt ohomogeniz e itan dt oremov e coarse material such asstones , remaining large clods and plant debris. Mesh size ofth e sieve depends on the dimensions ofth e cores (large aggregates are not suitablefo rsmal l cores) and the type ofstructur e onewant st oproduce . Sieving must be done ata gravimetri c moisture contentwel l below the lower plastic limit to prevent deformation ordisrup ­ tion ofaggregates . Eliminate the largerfauna l elements (meso- and macrofauna) byheatin g the soilt o 50°Cfo ra tleas t 30 minutes ina stove . Excessive drying ofth e soil shouldb e prevented by keeping iti na bo xo rplasti cbag . Condition thesoi l (bysprayin g orevaporating ) toth e moisture content atwhic h the artificial cores aret ob eproduce d and allow to reach anequilibrium . Atthi s point the prepared soil may be stored intightl y closed plastic bags atlo w temperature

73 (to slow down decomposition oforgani c matter) until iti sneeded . Weigh the calculated amount ofsoi l needed, pour ina cylinde r and compresst o the desired volume, using amechanica l press and astam p ofslightl y lesserdi ­ ameter than the diameter ofth e core. When the press can be adjusted tosto pa t the right height,ther e will be no needt ogaug e pressure.

5.3.Practica lconsideration s

- Asa pressur e gradient inevitably develops during compression, iti s recommended to distinguish upper and lower ends ofth e cores when they are used inexperi ­ ments. - Asth e pressure gradient develops stronger as higher cores are produced,th e ratio of height to diameter ofcompactio n layers may not exceed 0.5. - Depending on the properties ofth e soil used,th e corewil l expand more orles s after compression. Iti srecommendabl et otes t towha t volume compression should take placet oproduc e the desired volume. - Topreven t unequal distribution ofpressure , the soil and the stamp must be level when compressing. - Asheatin g to50° C affects nitrifying bacteria, itma y be advisable toad d cultureso f these after the heating process, if normal decomposition oforgani c matter iscon ­ sidered desirable. - To obtain an undisturbed soil core after the experiment, athi n (stiff) plastic ring may be mounted to the inner surface ofth e cylinder (Fig­ ure 5.1). Topus h the core out of the cylinder, astam p may be used witha diameter large enough toexer t pressuret oth e strip instead oft o the soil core. - Controlo fanimal s leaving orenter ­ ing the soil core can be realizedb y covering the open ends ofth ecylin ­ derwit h nylon gauze, secured to the cylinder with atigh t plastic ring Fiwe 5.1: Schematicdrawing of a cylinder (C) (Fiaure 51 ) usedfor the production ofartificial cores, withinner plastic ring (R) forobtaining undisturbedcores, nylongauze (G) and securingrings (S). See textfor further details. 74 5.4.Result s

Table 5.1 showsth ecoefficient s ofvariatio n insom ephysica lcharacteristic so f artificialcore sproduce dfro ma marin eloa msoi lcompare dwit hdat afo r undisturbed soilcore si nth esam eporosit y rangefro mth esam efield . Noteth ehig h uniformityo f theartificia lcores . Figure5. 2i sa photograp ho fa thi n sectionfro mth esam ekin do fcore ,i n whichth eoccurrin g pressuregradien ti s visible,causin gth elarges tpore st ob e founda tth eto po fth e core.

Table 5.1: Coefficientsof variationof several physicalparameters offield cores and artificialcores from a marine loam arable soil. Moisturecontent and air content measured at -0.01M Pa waterpotential. Fielddata fromAnonymous (1984).

Field cores Artificialcore s

Total porosity 6.26 0.41 Moisture content 4.94 0.78 Figure5.2: Thin sectionof an artificial corefrom Air-filled porosity 32.05 3.36 a marineloam arable soil. Totalporosity No. ofobservation s 560 19 46%. Naturalwidth 43.5 mm. Soilsieved witha mesh size of8 mm.

5.5. Discussion

Coresproduce di nthi swa yar ebein guse di nstructur erelate dresearc ho nroo t systems,e.g .b yBoon ean dVee n (1982),wh oals omanipulate d porestructur e inthes e coresb ymakin gartificia lmacropores . Didden (1987)use dth etechniqu et oinvestigat e thereaction s ofa nonychiuri dcollembola nt odifferen tdegree s ofsoi lcompaction . Didden (1990)studie dth einfluenc eo fenchytraei dactivit yo nsoi lstructur e usingthi s technique. Marinissen &Miedem a(i npress ) usedmulti-layere d cores producedb y thistechniqu et ostud ytunnelin g behaviour ofearthworms . Thetechniqu efurthe r offers possibilitiesfo rcreatin gartificia l barriers insoil ,e.g . to investigateth eeffec to fslakin go nsoi lfauna . Alsoartificia lmacropore sca nb eadde d tostud yth ereactio n ofroot sand/o rsoi l fauna.

75 6.Involvemen to f Enchytraeidae (Oligochaeta) insoi lstructur e evolution inagricultura l fields

Abstract

Theeffect so fenchytraei dactivit yo n soilstructur ewer erecorde di na fiel d studyo npopulatio n dynamicsi nagro-ecosystems ,an di na fiel dexperiment , usingartificiall y compoundedsoi lcores . Itwa sestablishe dtha t2 1- 35 % of theenchytraei dpopulatio ncontaine dminera lgrains . Theestimate dtranspor t ofminera lmateria li nth euppe r0. 4 mamounte dt o0.00 1 -0.0 1% ofth ebul k soilpe ryear . Inexperimenta lcore swit henchytraeid s present,th eai rper ­ meability,th evolum eo fpore si nth esiz eclas scorrespondin gt oenchytraei d bodywidth ,an dth eproportio n ofaggregate scorrespondin gt oth esiz eo fthei r fecalpellet swer ehighe rtha ni ncore swithou tenchytraeids .

6.1. Introduction

Theproble mo fsoi lstructur edeterioratio n isreceivin g increasedattentio ni nagri ­ culture. Itca nb eprevente d orcounteracte dt osom eexten t byth e structure-forming activitieso fsoi lanimals . Theinteraction s betweensoi lorganism san dsoi lstructur e arebein ginvestigate da sa par to fth eDutc hProgramm eo nSoi lEcolog yo fArabl e FarmingSystem s (Brussaarde tal. , 1988),th eobjectiv ebein gt oaccumulat ebasi c knowledgefo rth edevelopmen t ofecologicall y soundalternative st oconventiona l agriculturalpractices . Whensoi lstructur e isdefine da sth esiz ean darrangemen to f particlesan dpore s insoi l(Oades ,1984) ,th efollowin gaspect so ffauna linfluenc eo nsoi lstructur eca nb e distinguished:

1. Influenceo npor estructure ,i.e .o nsiz ean darrangemen to f pores, through: - enlargement,b yapplyin gpressur eo rtransportin g soilmaterial ; - reduction, forinstanc e by the fillingo f poreswit hmateria lfro melsewhere ,o r asa neffec t ofexterna lpressure ; - formationo fne wpore sb y burrowing.

76 2. Influenceo nsoi laggregate sthrough : - amechanica l reduction in size; - joining particleso raggregates ,e.g. ,a spar to fth eformatio no ffeca lpellets ; - changingth estabilit yo faggregates ,fo r instance byphysiologica lprocesse s indigestio no rsecretio no fmucilages .

Forearthworm si nparticular , manystudie shav ebee ndevote dt oth einfluenc eo f soilfaun ao nsoi lstructure . Theimportanc eo fearthworm s inth eformatio no fpores , andthu sthei r influenceo naeration ,drainage ,an drootability ,an di nth eproductio no f stableaggregates ,ha sbee nestablishe d beyonddoub t (Edwards& Lofty ,1977 ; Lee, 1985). Othergroup so fth esoi lfauna ,wit hth eexceptio no fant san dtermites , havereceive d muchles sattention . Yet,i tca nb eexpecte dthat ,b ythei rwa yo flife , manymember so fth esoi lfaun ama yinfluenc esoi lstructure ,suc ha smicroarthropod s contributing tohumu sformatio n (Zachariae,1963 )an ddun gbeetle saffectin gpor e structure (Brussaard& Hijdra ,1986) . Enchytraeidae (potworms)ar eon eo fth eleas t investigated groups,notwithstandin gthei rabundanc ei nman yhabitats . Jegen(1920 ) suggestedtha tthes eorganism s mayproduc ea nextensive ,b ei tspatiall yrestricted , burrow systemwit ha spong yappearance . Zachariae (1964),Babe l(1968) ,an d Pawluk (1987)hav ereporte doccasionall yver ylarg eportion s ofenchytraei dexcre ­ mentsi nmo ran d moderhumus ,bu tth einfluenc eo npor estructur e haslargel ybee n ignored (O'Connor, 1967)o rdenie d (Gómy,1984) ,an dth eenchytraei d influencevi a excrementsha sbee ndisregarded . Ina fiel dstud yo fth epopulatio ndynamic so f Enchytraeidaei nagro-ecosystem s (thisthesis) ,a considerabl e parto fth epopulatio ncontaine dgrain so f mineralsoil . To learnmor eabou tth esignificanc e ofenchytraei dactivit yfo rvariou saspect so fsoi l structure,a fiel dexperimen twa scarrie dout . Thischapte r reportsth efiel ddat aan d the resultso ftha texperiment .

6.2.Method san dmaterial s

6.2.1. The experimental field

Bothth efiel dsamplin gan dth efiel dexperimen twer ecarrie dou to nth e experi­ mentalfar m'Dr . H.J.Lovinkhoeve 'i nth eDutc h Noordoostpolder, reclaimed in1942 . Thecultivate d layer isa sil tloam ,wit ha sil tfractio n (particles< 1 6um ) of30% , 10% calciumcarbonate ,an dp H(KCl ) 7.5. Belowapproximatel y2 5c mther ei sa laye ro f veryfin eloam ysand .Th eyearl yrainfal li s65 0- 80 0mm . Since198 6th ecro protatio n hascomprise dwinte rwhea t- suga rbee t- sprin gbarle y- potatoes .

77 6.2.2. The field sampling

FromApri l 1986u pt oan dincludin gApri l1988 ,sample swer etake nt oa dept ho f 40cm ,mostl ya tmonthl yintervals ,i ntw ofield sa tth eLovinkhoev eexperimenta lsite , field 12B,conventionall ymanaged ,an dfiel d 16A, witha nintegrate dmanagement . 'Conventional'i suse dt odenot eploughin gt o2 5c man dhig hinput so ffertilize ran d pesticides. 'Integrated'mean sa reduce dploughin gdept h(1 5cm )an dlowe rinput s of fertilizeran dpesticides . Theorgani cmatte r contenti nth euppe r20-2 5c mo fth etw o fieldswa s2.3 %an d2.9% ,respectively . Adetaile ddescriptio no fth esamplin gmetho d andth estud yare ai sgive nelsewher e (Kooistrae tal. , 1989;chapte r3 o fthi sthesis) . Atth eLovinkhoev eexperimenta lsite ,dail yrecording swer emad eo fprecipitatio nan d airtemperature . Theextracte dpotworm swer eindividuall yexamine dunde ra microscope , meas­ uredt oth eneares tmm ,an didentifie dt ospecies . FromJun e198 6onward sth epres ­ enceo fminera lmateria l inth egu tconten twa srecorde ddurin gth eexaminatio ni n threeclasse sa sno ,fe w (occupying lesstha n 1/4o fth ebod ylength) ,o rman y(mor e than1/ 4 ofth ebod ylengt hoccupied ) mineralpart spresent . Toestimat eth equantit yo f mineralsoi lpresen t inth epopulatio n ata sampl edate ,i twa sassume dt ocompris e quartzgrain swit ha diamete ro f6 0ur n (Babel,1968 )an da specifi cmas so f 2650k g m3,an dtha tpe rm mbod ylength ,on esuc hgrai nwa spresen ti nanimal swit h few,an dtw oi nanimal swit hmuc hminera lmaterial . Tocalculat ea nestimat eo fth e quantityo f mineralsoi ltransporte dpe ryea rb yth eenchytraeids ,i twa sassume dtha t themea no fth eestimate damount spe rsampl edat ewa spresen tthroughou tth eyear . Further,a nestimat eo fth eturnove rtim eo fth egu tconten twa sneeded . Takinga sa n indicationth efigure so f Bolton& Phillipso n (1976),wh ofoun da gu tturnove rtim eo f 1- 2.5 hfo rth elumbrici dAllolobophora rosea, itwa sassume dtha to naverag eth e turnovertim ewa s2 h .

6.2.3. The field experiment

Artificialsoi lcore swer eproduce di nPolyvinylchlorid e cylinders,wit ha ninne r diametero f4 2m man da heigh to f2 5mm . Onth einne rsurfac eo fth ecylinder sa stif f plasticstri p(Elastotherm ,0. 5mm )wa smounted ,reducin gth einne rdiamete rt o 41mm . Thisstri pwa suse dt opus hth ecor eou to fth ecylinder swithou tdisturbin gth e soilstructure . Thesoi luse dwa scollecte dfro mth eploughe dlaye ra tth eLovinkhoev e experimental site,afte rtillage . Thesoi lwa sfroze n (-40°C)t oimitat eth eactio no ffrost . Bysievin g (wiregauz esieve ,8 m mmesh-size ) thesoi lwa shomogenize dan dcompo ­ nentstha tcoul dhinde rth eproductio no fth ecore s (likestones ,coars eorgani cmateria l

78 andlarg esoi laggregates ) wereremoved . Thesoi lwa sthe nheate dt o50° Cfo ra tleas t 30min ,t oeliminat emacro -an dmesofaun awithou tkillin gal lmicro-organisms . The preparedsoi lwa sstore di ntightl yclose dplasti cbag sa t4°C . Toproduc eth eartificia lsoi lcores ,th emoistur econten to fth esoi lwa sadjuste dt o 22.5%b yweight ,an d54.3 9g soi lwa scompresse di na cylinder . Tohal fo fth enumbe r ofcore sproduced ,0. 5g sieve d(0. 3mm )oa tbra nwa sadde dbefor ecompression ,t o raiseth econten to fdecomposabl eorgani cmateria li nth esoils . Thesoi lcore spro ­ ducedi nthi swa yha dair-fille dpor evolume sa ta wate r potentialo f -0.01MP ao f13. 4 and 12.1% ,respectively ,wit ha standar ddeviatio no f0.9 %fo rbot htypes . Thephysica l characteristicso feac htyp eo fsoi lcor ewer ehighl yunifor m (Didden,1987) . Three-quarters ofth esoi lcore swer esupplie dwit hfiv efres hcocoon so f Enchytraeusbuchholzi 'from laboratoryculture sbefor eth ecore swer ebrough tint oth e field. Theope nend so fth ecylinder swer ecovere dwit hnylo ngauz eo f4 0ja m mesh- size,whic hwa ssecure dt oth ecylinde rwit ha tigh t plasticring . Thismes hsiz ewa s consideredsufficien t topreven teve nth esmalles tenchytraeid sfro mleavin go renterin g thecylinders ,whil ea tth esam etim ewate r movementthroug hth esoi lcore swa sno t impeded. Thesoi lcore swer ethe nadjuste dt oa wate rpotentia lo f-0.0 1 MPaan dthei r airpermeabilitie s (accordingt oKmoch ,1961 )determined . Inall ,51 2soi lcore swer eproduce di nthi sway ,38 4o fwhic hwer esupplie dwit h potworms. Inth ecours eo f3 week si nNovembe r 1987the ywer ebrough t intoth efiel d atth eLovinkhoev eexperimenta lsite . Soilcore swit ha slightl ylarge rdiamete rtha nth e outer diameter ofth ecylinder swer eextracte dwit ha stee lcorer . Theartificia lcore s wereplace di nth ehole ,an dth ehol ewa sclose dwit hpar to fth epreviousl yremove d soilcore . Theplac eo fth ecylinder s inth efiel dwa smarke dwit hsmal lstick swit h colour bandstha tindicate dth etyp eo fcor eunderneath . Duringth eexperimen tth esoi l waskep tfallow . Halfth esoi lcore swer eburie da ta dept ho f2. 5c m(fro mth eto p of thecylinder) ,th eothe rhal f at7. 5 cm. Inth ecours eo fth eexperimen t noclea rdiffer ­ encesbetwee nthes etw ogroup semerged ;the yar etreate da son egrou pan danalyze d asa 2x 2factoria lexperiment ,th efou rtreatment sbeing :

1. Withoutpotworms ,withou toa t bran; 2. Withpotworms ,withou toa tbran ; 3. Withoutpotworms , withoa tbran ; 4. Withpotworms ,wit hoa tbran .

FromJanuar y 1988onwards ,6 4soi lcores ,8 fro meac ho fgroup s 1an d3 an d2 4 fromeac ho fgroup s2 an d4 ,wer eselecte dever ymont ha trando man dtake nou to fth e field. InJul y198 8th eexperimen twa sterminate dwit hth eremova lo fth eremainin g 128 cores. Theremove dsoi lcore swer eadjuste dt oa wate r potentialo f-0.0 1MP aan dthei r airpermeabilitie s determined. Tokee ptrac ko fth epopulatio ndevelopmen t ofth e

79 enchytraeids,1 6(i nJuly :32 )core sfro mgroup s2 an d4 wer eextracte deac h month. Toth eremainin g8 (i nJuly : 16)soi lcore spe rgroup ,treatment swer eapplie da sout ­ linedi nTabl e 6.1.

Table 6.1: Treatmentsapplied to eachexperimental group of soil cores in thecourse of the experiment

Month Impregnation Determination of Determination of aggregatestabilit y water retention characteristics

January 4 February 4 4 March 4 4 April 4 4 May 4 4 June 4 4 July 4 6 6

6.2.4.Treatment s infiel d experiment

Extraction procedurefollowe dO'Conno r(1967) ,wit hsligh tmodifications . Thesoi l coreswer elef ti ncol dwate rfo r3 0min ,afte rwhic hth eligh tintensity ,an dthu sth eheat , wereslowl yincrease dt oreac ha maximu mo fapproximatel y60° Ci n 150min . The totalextractio ntim ewa sthu s18 0min . Impregnationfollowe dth emetho ddescribe db yMiedem ae tal . (1974),afte r transferringth ecore sundisturbe dfro mth ePolyvinylchlorid ecylinder st ostainles sstee l cylinderso fth esam einne rdiameter . Afterth e resinha dhardened ,th ecore swer e sawnlongitudinall y andpolished . Theywer estudie dunde ra binocula r microscopea t upt o4 0x magnification . Forth edetermination so faggregat estability ,th ewe tsievin gmetho d (Burkee tal. , 1986)wa suse dwit hsligh t modifications. Theair-drie dcore swer ecare ­ fullycrumble d andth esoi lwa ssieve dint oth efraction s0.1 5- 0.3,0. 3- 0. 6an d 0.6- 1 mm. Eachfractio nwa splace do nto po fa nes to fsieve swit hdecreasin g mesh-size,slowl yimmerse di nwater ,an dcarefull ymove dt oan dfr ofo r5 mi ni na standardizedway . Afterwards,th eamoun to feac hfractio nint owhic hth eaggregate s fellapar twa sdetermine db ydryin gan dweighin gth eamoun to fsoi li neac hsieve . The figuresuse di nth ecalculation swer eth epercentag elef ti n theuppe rsiev ean dth e meanweigh tdiamete ro fth eaggregate s inth enon-stabl eportion . Eachdeterminatio n wascarrie dou ti nduplicate .

80 Thewate r retentioncharacteristic swer edetermine dafte r heatingth esoi lcores , wrappedi nplastic ,fo ra tleas t3 0mi na t50°C ,t oterminat eth eactivitie so fth epot - worms present. Measurementswer emad ei nth erang e-0.00 1t o -0.01 MPa water potential,representin gequivalen t porediameter so f30 0- 3 0jum ,o nsan dplates .

6.3.Result s

6.3.1. The field sampling

Table6. 2list sth epercentage so fth epotwor mpopulatio ncarryin gminera l grainsan dth ecorrelation swit hmea nai rtemperatur ean dtota lprecipitatio nfo rvariou s depths. Atal ldepths ,th epercentag eo f potwormscarryin g mineralmateria li nth egu t wasles si nth eintegrate dfield ,th edifferenc e beingsignifican t (P<0.005,t-test )fo rth e 10- 2 5an d2 5- 4 0c mlayer san dfo rth e sampleddept ha sa whole . Inbot hfield s therewa sa negativ ecorrelatio nwit htemperatur e [significanta tth e5 %level ,excep tfo r the1 0- 2 5c mlaye r in theintegrate dfiel d(16A )an dth e0 - 5 c mlaye r in theconven ­ tionalfiel d (12B)]. Therewa sa sligh tpositiv ecorrelatio nwit hth eamoun to fprecipita ­ tion (significanta tth e5 % levelonl yfo rth e5 -1 0 cmlaye ri nth eintegrate dfiel dan dth e 10- 2 5c mlaye r in theconventiona lfield) .

Table6.2: Percentages of thepopulation carryingmineral grains, averaged for variousdepths over thesample period, and thecorrelations withmean air temperature(Rnwp) and totalprecipitation (Rp*c) ofthe 3 weeks preceding asampling

Field16 A Field 12B (integrated) (conventional)

Depth (cm) 0-5 5-10 10-25 25-40 0-5 5-10 10-25 25-40

%wit h grains 15.5 18.7 23.8 28.8 28.3 21.7 38.0 40.8

nTemp -0.25 -0.47 -0.15 -0.28 -0.08 -0.27 -0.37 -0.33 Probability 0.016 <.001 0.129 0.006 0.560 0.021 <001 0.004

Rprec 0.19 0.20 0.16 -0.02 0.03 0.15 0.20 0.21 Probability 0.072 0.049 0.097 0.882 0.800 0.220 0.038 0.071

81 Table6. 3present sth erelativ eabundanc eo fth emos tabundan tspecie san d the percentages ofthei rpopulation scarryin g mineralgrains . Thistabl eshow sappreciabl e differences betweenspecie si nth ecarriag eo f mineralmaterial . ForEnchytraeus buchholzi, thedominan tspecie si nbot hfields ,th epercentag eo fanimal scarryin g mineralgrain swa sles stha n2 0i nbot hfields , whereasth eothe rspecie swer erela ­ tivelymuc hmor einvolved . Inth econventiona lfield ,al lspecie scarrie dminera lmate ­ rialt oa large rexten ttha ni nth eintegrate dfield ,th edifferenc e beingsignifican ta tth e 5%leve l(t-test )fo rEnchytraeus buchholzi an d Fridericia sp. Ban dhighl ysignifican t (P<0.001,t-test )whe nal lspecie swer eanalyze dtogether .

Table6.3:The most abundantspecies at the Lovinkhoeve experimental site, theirrelative abundance (aspercentage oftotal population), andthe percentage of theirpopulation carryingmineral grains, averaged overthe sample period, layer 0-40 cm

Field 16A (integrated) Field 12B (conventional) Species Relative Percentage with Relative Percentage with abundance mineral grains abundance mineral grains

Enchytraeus buchholzi 65.3 12.2 57.3 18.5 Henleaperpusilla 8.3 32.6 7.2 39.5 Fridericiasp. A 9.9 33.7 3.1 35.0 Fridericiasp. B 10.3 54.3 27.0 70.2

All species 21.2 35.4

Theestimate dquantitie so fminera lsoi ltransporte db yth eenchytraei dpopulatio n duringth esamplin g periodar egive ni nTabl e6.4 . Here,th eestimate sfo r 1986 and 1987ar ecalculate dseparatel y becausei nth ewe tsumme ro f 1987th enumber s of potworms,an dthu sth eestimate so fminera lmateria ltransported ,wer emuc hlarger . Generally,mor eminera lsoi lwa stransporte d inth econventiona lfiel d (12B). In the upper1 0c mo fth eprofile ,however ,mor emateria lwa stransporte d inth eintegrate d field (16A). Expresseda sa proportio no fth ebul ksoi lvolume ,th etranspor ti nbot h fieldswa si nth eorde ro fmerel y 0.001 -0.0 1% .

Table6.4: The estimatedquantities (g/rrf/year) ofmineral soil transportedby the enchytraeid population atvarious depths

Field 16A (integrated) Field 12B (conventional) Depth (cm) 1986 1987 1986 1987

0-5 1.1 10.3 0.7 4.1 5-10 0.9 5.4 0.8 6.9 10-25 4.8 16.7 6.3 37.6 25-40 3.5 9.1 6.5 26.3

0-40 10.3 41.5 14.3 74.9

82 6.3.2. The field experiment

Figure6. 1 showsth epopulatio ndevelopmen to fth eenchytraeid s inth eexperi ­ mentalsoi lcore stogethe rwit hth epercentag eo fthei r population involvedi nth etrans ­ porto f mineralmaterial . Therewa sa significan t negativecorrelatio nbetwee nthi s percentage (P=0.003fo rcore swithou toa tbran ,P<0.00 1fo rcore swit hoa tbran )an d themea nai rtemperatur efo rth e3 week sprecedin gth e sampling.

to o

(0 a

CO 0) 0 c e c

o> rcs *-> c Ü i_ CD a

Apr May

Figure6.1: Population developmentof enchytraeidsin experimentalcores (bars) and thepercentage ofanimals (lines)in the population containingmineral particles. Barsrepresent numbers (naturallogarithms) per core

Withoutoat bran With oatbran

Inth e coreswithou toa t bran,populatio ndevelopmen tstarte dearlier , resulting in significantly moreenchytraeid s (P=0.05,Mann-Whitne ytest ) onth efirs tsamplin g occasion,i nJanuar y 1988. Subsequently,th epopulatio ndevelopmen twa smos t extensivei nth ecore swit hoa tbra nadde d(P<0.05 ,Mann-Whitne ytest ,excep ti n Marchan dJuly) . Iti slikel ytha tth edeclin eo fth epopulatio nafte r May198 8coincide d withdepletio no fth eavailabl efood . Throughoutth eexperimenta l period,th epercent ­ ageo fth epopulatio ncarryin gminera lgrain swa slarges ti nth esoi lcore swithou toa t

83 bran. Inbot htypes ,th ehighes tpercentage soccurre d inth eperio dJanuar ythroug h April. Theactua lnumber so fanimal scarryin gminera lgrain sremaine dfairl yconstan t inth esoi lcore swithou toa tbran ,whil ei nth ecore swit hoa tbra nth ehighes tnumber s werefoun di nth eperio dfro mApri lthroug hJune . Thetota lweigh to ftransporte dmin ­ eralsoi li nth eexperimenta lperiod ,usin gth esam eassumption s asabove ,wa sesti ­ mateda s0. 5 mg forth e coreswithou toa tbran ,an d3. 5m g forth ecore swit hoa t bran, whereth epopulatio n developmentwa smuc hmor eextensive . Expressed aspercent ­ ageso fth etota lcylinde rvolum eo na yearl ybasis ,thi srepresente d0.00 1 and0.004% , respectively.

2.0 2.0 Without oat bran With oat bran

1.5

» 1.0

I 0.5

0.0 1l a Jan Feb Mar Apr May Jun Jul Jan Feb Mar Apr May Jun Jul

Figure6.2: Air permeability in experimentalcores, relative to values determined at start of experiment. *:P<0.01, significant difference in pairs, Mann-Whitney test

Withoutpotworms Withpotworms

Theinfluenc eo fth epotworm so nth epor estructur eo fth esoi lcore swa sreflecte d inth emeasurement so fai rpermeabilit y andth ewate r retentioncharacteristics . Fig­ ure6. 2show sth echange s inai rpermeability ,relativ et oth evalue sdetermine da tth e starto fth eexperiment . Inth ecore swithou toa tbra nai rpermeabilit y initiallydeclined , followedb ya ris efro mApri lonward st oapproximatel yth estartin gvalues . Thistren d wasstronge r inth ecore swit hpotworm spresent ,th edifferenc e beingsignifican ti n Aprilan dMa y(P<0.05 ,Mann-Whitne ytest) . Inth ecore swit hoa tbra nthi s patternwa s morecomplicated ,wit ha nadditiona lris ei nai rpermeabilit y inFebruar y inth ecore s withoutpotworms ,an dth edifferenc e betweencore swit han dwithou tpotworm sno ta s consistentfro mApri lonward sa si nth ecore swithou toa tbran . Table6. 5sum su p the resultso fth eanalysi so fvariance ,carrie dou tseparatel y onth ecore swit han dwithou t

84 Table6.5: Results of the analysis of variance(P values) of measured airpermeability in coreswith and withoutoat bran

Source ofvariatio n Without oat bran With oat bran

Time <0.001 <0.001 Enchytraeids 0.004 0.692 Interaction 0.622 0.003

15 r

i_ O a

Figure 6.3:Pore volumes (sizeclass 50• 200 urn), calculatedfrom waterretention characteristics, in thecourse of the experiment

Withoutoat bran: Withoutpotworms Withpotworms With oatbran: m Withoutpotworms Withpotworms

85 oatbran . Inbot htype so fcore sth eeffec to ftim ewa shighl ysignificant ;i nth ecore s withoutoa tbra nther ewa sals oa significan teffec to fpotworm san di ncore swit hoa t brana significan t interaction betweentim ean dpotworms . Fromth ewate rretentio ncharacteristic sth epercentage s (byvolume ) ofsevera l poresiz eclasse swer ecalculated . Figure6. 3present sth eresult sfo rth esiz eclas s 50- 20 0 Mm. Incore swit hoa tbra nth epor evolume s inthi ssiz eclas swer eo naver ­ age0.85 %highe rwit hpotworm spresen t(P=0.059 ;analysi so fvariance) . Insoil s withoutoa tbra nan di nothe rsiz eclasse sn osignifican teffect swer edetected . Amicroscopi cstud yo fth eresin-impregnate d coresshowe dtha tth eactivit yo fth e potwormswa scleares ta tth eperipher yo fth elarge rsoi laggregates . Atth estar to fth e experimentthes ewere ,a sa consequenc eo fth eproductio ntechnique ,mor eo rles s rounded. Probablya sa resul to fth eremova lo f materialfro mth eperipher yo fth e aggregatesb yth eenchytraeids ,thi sshap echange dt oa mor eirregula rfor m(Fig .6.4) .

Figure 6.4:Indications ofenchytraeid activity in experimentalcores with oatbran added; photographs frompolished blocks, withincident light; width of view4 mm. Left,a core at the startof theexperiment; Right, acore with enchytraeidsafter 6months in the field

Inal ltreatment saggregat estabilit ydecline di nth ecours eo fth eexperiment . Figure6. 5show sth eaggregat estabilitie s andmea nweigh tdiameter so fth enon-stabl e portionfo rth e sizeclasse s0. 6- 1 mman d0. 3- 0. 6 mm. Table6. 6list sth e Pvalue si n theanalysi s ofvariance . Incore swithou toa tbran ,th eaggregate s inbot hsiz eclasse s weregenerall yles sstabl ewhe npotworm swer epresent ,bu tth edeclin e inth ecours e oftim ewa sals oless . Inth esiz eclas s0. 6- 1 mmth emea nweigh tdiamete r ofth e non-stableportio n becamesmalle r inth ecours eo fth eexperiment ,bu tles ss owit h enchytraeids present. Inth ecore swit hoa tbra nn oclea rtendencie swer edetected .

86 Stability 0.6 — 1 mm 50%

0% • mW MWD 0.6 — 1 mm 0.2 mm

0 mm Stability 0.3 - 0.6 mm 50%

0% MWD 0.3 - 0.6 mm 0.2 mm

0 mm Jan Mar May Jul

Figure 6.5: Courseof aggregate stability andmean weightdiameter (MWD)of the non-stable portion for thesize classes 0.6• 1 mm and 0.3• 0.6 mm

Withoutoat bran: Withoutpotworms Withpotworms

With oatbran: Withoutpotworms Withpotworms

Table6.6:Results of the analysis of variance (P values) for thestability of aggregatesin thesize classes 0.6-1 and 0.3-0.6mm, and themean weightdiameters (MWD) ofthe non-stable portions

soil aggregates 0.6- 1 mm 0.3- 0.6 mm Stability MWD Stability MWD

Without oat bran:Tim e <.001 <.001 <.001 0.239 Enchytraeids 0.006 0.219 0.034 0.464 Interaction 0.001 0.010 0.036 0.368 With oat bran: Time <.001 0.002 <.001 0.008 Enchytraeids 0.624 0.068 0.964 0.146 Interaction 0.356 0.559 0.875 0.101

87 6.4.Discussio n

Therewa sa napparen tdifferenc e betweenth etw ofield s usedi nth efiel dsamplin g inth eestimate damount so fminera lmateria ltransporte da tvariou sdepths .I n the conventionalfiel d mostmateria lwa stransporte di nth edeepe r (10-40 cm)layer , while inth eintegrate dfiel dth eto playe rwa saffecte dt oa greate rextent . Althoughth etota l amounttransporte dwa shighe ri nth econventiona lfield ,thi sma yimpl ytha tth einflu ­ enceo fenchytraei dactivit yo ncondition sfo rgerminatio no fseed san do nsoi laeratio n isstronge r inth eintegrate dfield . Thenegativ ecorrelation ,foun dbot hi nth efiel dsamplin gan di nth eexperiment , betweenth emea nai rtemperatur ean dth epercentag eo fanimal scarryin gminera l grains,remain sa phenomeno ntha trequire sexplanation . Therema yb ea chang ei n feedingbehaviou ri nrespons et otemperatur echanges . Assumingtha tenchytraeid s feedmainl yo nmicroflor a (Toutaine tal. , 1982) iti spossibl etha ta thighe rtempera ­ tures,whe nth emicroflora lgrowt ho norgani cmateria li shigh ,thi smateria l ispreferen ­ tiallyselected . Atlowe rtemperature s itwoul db enecessar yfo rth eanimal st ofee d indiscriminately, ingesting mineralgrain salso ,t ob eabl et oobtai nenoug hfood . Therewa sgoo dagreemen tbetwee nth epercentage so fanimal scarryin gminera l materiali nth efiel dsamplin gan di nth efiel dexperiment . Thisals ohel dfo rth eesti ­ mateso fth eamount so f mineralmateria ltransported , whichi nal lcase swa si nth e ordero f0.0 1t o0.00 1% ofth esoi lvolume . Bothi nth efiel dsamplin gan di nth efiel d experimentth epercentag eo fth epopulatio n carrying mineralmateria lwa slowe rwhe n theorgani cmatte rconten twa shigher ,indicatin gtha tenchytraeid sfee dmor eselec ­ tivelyo norgani cmatte rwhe nthi si savailable . Inth eexperimenta lcore stha t hadoa t branadded , theamoun to ftransporte dmateria lwa snevertheles shigher ,becaus eo f themuc hlarge rpopulation s inthes ecores . Thedecreas ei naggregat estabilit ywit htime ,occurrin g inal ltreatments ,ma ywel l agreewit hth efinding so fGuid ie tal . (1988),wh ofoun da clea rseasona lfluctuatio ni n aggregatestability . Inth esoi lcore swithou toa tbra nth eactivit yo fenchytraeid sle dt o agenerall ylowe raggregat estabilit yi nth esiz eclasse s0. 6- 1 and0. 3- 0. 6 mm. How­ ever,th estabilit yo fthes eaggregate san dth emea nweigh tdiamete ro fth enon-stabl e portioni nth e0. 6- 1 mmsiz eclas sdecrease dfaste r inth ecours eo ftim ewhe nn o enchytraeidswer epresent . Theseresult s indicatetha tthes eaggregate s mighthav e beenpartl ycompose do ffairl ystabl eenchytraei dexcrements ,wit ha diamete r ofabou t 0.2mm . Nosuc heffect swer edetecte di nth ecore swit hoa tbra nadded ,i nspit eo fth e larger populationso fpotworm si nthes ecores ,wher eth estabilizin geffec t ofth eadde d organicmatte r mighthav emaske dthei r influence. Another possibility istha tth eprop ­ ertieso fth eexcrement swer einfluence db yth ekin do ffoo dconsumed ,a sfoun dfo r (Shipitalo &Protz ,1988) . Thechange s inai rpermeabilit ytha toccurre di nth efiel dexperiment ,sugges ttha t Enchytraeusbuchholzi influence dth epore-siz edistributio no rpor econtinuity . In the soilcore swit hoa tbra nadded ,ther ewa sa nincreas eo fabou t0.85 % inpor evolum e for poresi nth esiz eclas s5 0- 20 0um , indicatinga ninfluenc eo npor esiz edistribution . Thenon-significan t interaction betweentim ean dpotworm si nth esoi lcore swithou toa t branagree swit hth efairl yconstan tnumbe ro fanimal scarryin g mineralgrains . Asai r permeability isver ysensitiv et ochange s inpor esiz ean dpor econtinuity ,enchytraeid s mayaffec t either oneo rbot haspect so fsoi lstructure . Atth esam etime ,th eestimate d amounto f mineralsoi ltransporte d peryea rb ypotworm swas ,bot hi nth efiel dsamplin g andi nth efiel dexperiment ,i nth eorde ro f magnitudeo fonl y0.00 1- 0.0 1% ofth ebul k soilvolume . Intryin gt oreconcil ethi sapparen tcontradiction ,th efollowin gshoul db e kepti n mind.

1. Poresiz edistribution s asdetermine dfro mwate rretentio n curvesar e equivalent poresiz edistribution s andpor eneck spla ya nimportan t rolei nth ecalculate dpor e volumes (Bouma,1977) . Removalo f poreneck sma ychang eth eequivalen tpor e sizedistributio nan dgiv ea bette r porecontinuity ,withou tmuc hmateria lbein g removed. 2. Enchytraeids dono tonl ytranspor tminera lgrains . Duringfeeding ,organi cmate ­ riali sals otransported . Inth esoi lcore swit hoa tbra nadded ,th eris ei npor e volume inth esiz eclas s5 0- 20 0M m mayhav ebee npartl ydu et oth eclearin go f poresfro mth eoa tbran . Atth esam etime ,excrement sar eproduce dan ddepos ­ itedi nth esoil ,whic hma yals oinfluenc eth eequivalen t pore-sizedistributio nan d porecontinuity . 3. Anotherwa yt oproduc echange si npor estructur e isb yapplyin gpressur et oth e porewalls ,thereb yenlargin gsom ean ddiminishin gothers .

Apreliminar ymicroscopi c studyo fpolishe d blockso fenchytraeid-reworke d soil hasconfirme dtha t removalo fpor eneck si sa likel ymechanism . Further analysiso f theblock swil l be undertaken. Iti sconclude dtha t enchytraeids maycontribut esignificantl yt oth eevolutio no fsoi l structure inagro-ecosystems . Althoughactiv eburrowin g iso f minorimportanc ei n view ofth elo wquantitie s ofsoi ltransported ,enchytraeid s increase porecontinuity ; raiseth e volumeo fpore so f asiz ecorrespondin gt othei r bodysize ;an drais eth eproportio no f aggregatescorrespondin g toth esiz eo fthei rfeca lpellets . Foragricultura l practice,thi s maymea nbette r rootability ofth esoil ,bette raeratio nan da reduce dsensitivit yt o slaking. Theseeffect swil lb estronge rwhe nenchytraei dactivit yi sconcentrate d inth e upperlaye ro fth esoil ,a si sth ecas ei nfield swit hreduce dtillag edepth .

89 7.Synthesi s

Thecentra lquestion swit hwhic hthi sstud ystarte dou twere :

1. Whatd o Enchytraeidae contributet osoi lstructur eevolutio ni ndifferentl ymanage d agriculturalfields ? 2. Whati sth esignificanc e ofenchytraei d populations indifferentl y managedagricul ­ turalfield sconcernin gdecompositio n oforgani c matteran dnutrien tdynamics ?

Anevaluatio n ofth ecurren tknowledg eo nth eecolog yo fterrestria lenchytraeid s learned,tha trelativel y littledat ao nthes equestion sar eavailable ,th epaucit yo finfor ­ mationmainl yoriginatin gfrom :

- Thecomparativel y latestar to fecologica lstudie so nenchytraeids ,that , moreover, werelargel yconducte d innatura lhabitats . - Thesmal lnumbe ro fecologica lstudie s addressingthi soligochaet efamil yo nth e species level,an dth eresultin g lacko fdat ao nspecies-related ,ecologica lcharac ­ teristicslik efoo dpreference ,ecologica lstrategies ,life-history ,an denergetica l efficiency.

Asa corollar y ofthi slac ko fspecifi cknowledge ,a nattemp tt oquantif yth eecologi ­ calsignificanc eo f enchytraeid populations hast orel yo nth egeneralizatio n ofdat ao na fewspecie so ro ngenera lassumption s aboutthi sfamily . Therefore,th enee dfo r fundamentalecologica lresearc ho nth especie s levelwa sstressed ,an dsom ebasi c researchwa s conducted.

Inthi sthesis ,basi cecologica ldat aar egive no nlength-weigh t relationso fth e enchytraeidspecie soccurrin ga tth eLovinkhoev eexperimenta lsite ,an do nth elife - historyo fEnchytraeus buchholzi. Inpresentin gth elife-histor y data,th eproblemati c charactero fth etranslatio no f laboratoryresult st ofiel dsituation sha sbee nemphasize d bycomparin gprediction sfro mth elaborator ystud ywit hobservation sfro martificia lsoi l cores. Itappeared ,tha tth epopulatio ndevelopmen to fthi sspecie sunde rfiel d condi­ tionscoul ddeviat estrongly , bothnegativel yan dpositively ,fro m predicteddevelop ­ ment.

Theresult so f populationdynamica lan dproductio necologica lresearc hconducte d atth eLovinkhoev eexperimenta lsite ,mad ei tclea rtha t theenchytraeid s constituteda noteworthyfauna lgrou pi nth efou rfarmin gsystem sstudied . Itwa scalculated ,tha tth e enchytraeidpopulation s respired0.5-3.7 %o fth eorgani ccarbo ninpu tt oth esystems ,

90 andtha tth enitrogen-flu xthroug henchytraei dbiomas samounte dt o0.19-0.6 0g N/m 2/ yr- Generally,ther ewer en osignifican t differences betweenth esystem sstudied , as regardsspecie scomposition ,populatio ndensities ,biomas san dproductio n ecological parameters. Therewere ,however ,significan tdifference s concerningth evertica l distri­ butiono fth eenchytraei dpopulations . In fieldswit hintegrate dmanagement ,th e popu­ lationswer egenerall yconcentrate di nth euppe rlayer so fth esoi lprofile ,wherea si n theconventionall y managedfiel dpopulation swer emor euniforml ydistributed ,o reve n concentrated indeepe rlayers . Thesedifference swer eassociate dwit hdifference s in tillagepractices ,whic hresulte di ndifference s inth edistributio no f plantremains . Thesephenomen awer eals oobserve di ndat ao fvariou sothe rgroup so fsoi l organ­ ismso nth esam esit e (Brussaard etal ,1990) .

Thusfar ,n oquantitativ e researcho nth eeffect s ofenchytraeid so nth eevolutio no f soilstructur eha dbee nconducted ,notwithstandin g theabundanc eo fenchytraeid si n manyhabitats ,an donl yconjecture s andqualitativ eindication sexisted . Inthi sthesis ,a methodwa spresente dt ostud yinteraction s betweenenchytraeid s andsoi lstructur e undercontrolled ,near-natura lconditions . Forthis ,artificia lsoi lcore swer eproduced , thatha da reproducibl ean dlargel ypredefine dsoi lstructure . Theeffect so fenchytraei d activityo nsoi lstructur ewer erecorde di na fiel dexperiment , usingsuc hartificiall y composedsoi lcores ,an di na fiel dstud yo npopulatio n dynamics. Itwa sestablishe d that inth eexperimenta l coreswit henchytraeid s present,th eai rpermeability ,th evol ­ umeo f poresi nth esiz eclas scorrespondin g toenchytraei d bodywidth ,an dth epropor ­ tiono faggregate s corresponding toth esiz eo fthei rfeca lpellet swer ehighe rtha ni n coreswithou t enchytraeids. Fromth efiel dstud yi tappeare dtha t2 1- 35 %o fth e enchytraeidsi nth eLovinkhoev epopulation scontaine dminera lparticles ,an dhenc e wereinvolve d intranslocatio n ofthi smaterial . Theestimate dtranspor to fminera l materiali nth euppe r0. 4m ,however ,amounte dt oonl y0.00 1- 0.0 1% o fth ebul ksoi l volumepe ryear . Therewa sa napparen tdifferenc e betweenth econventiona lan dth eintegrate d farmingsystem si nth ecalculate d amountso f mineralmateria ltransporte d atvariou s depths.I nth econventiona lfiel dmos tmateria lwa stransporte di nth edeepe r (10-40 cm)layer ,wherea si nth eintegrate dfiel dth eto playe rwa saffecte d toa greater extent. Hence,thi sphenomeno nwa sals oassociate dwit hth edistributio no f plantremains .

Although untilno wonl yfe wstudie s havequantitativel yaddresse dth eeffec to f Enchytraeidaei narabl esystems ,an dth evariou sstudie sca nno tb ecompare ddirectly , somegeneralitie s areapparent : - Enchytraeids playa nappreciabl erol ei nth eflow so f energyan dnutrient si n agroecosystems. Directcontributio nt otota lsoi lmetabolis m isi nth eorde ro f

91 magnitudeo fonl y1 % ,an di ssimila rt otha ti nmor enatura lhabitat s (Golçbiowska& Ryszkowski ,1977 ;Parmelee , 1987;Lagerlö f etal. , 1989;thi s thesis). Indirecteffect s (notablythroug hthei r influenceo nmicrobia lactivity ) probablywil lb emuc hhigher . Nitrogenflu xthroug henchytraei dbiomas sma y amountt o0. 1- 1 gN/m 2/yr(Paustia ne t al., 1990;thi sthesis) ,an dprobabl ywil l behighe rwhe nth eproductio no f excretaar etake nint oaccoun t(Chris - tensen,1988) . Thetota lcontributio n (directan dindirect ) ofenchytraeid st onitro ­ genmineralizatio n hasno tye tbee nestablishe d inagroecosystems ,bu tresult s frommicrocos mexperiment s suggesttha tenchytraei d activityma yenhanc e nitrogen mineralization bya smuc ha s18 %(Abrahamsen ,1990) . - Enchytraeids affectsoi lstructur eevolutio nthroug hth eproductio n ofexcrement s andmucilage s (Babel,1968 ;Pawluk ,1987 ; thisthesis) ,tha t mayhav ea stabiliz ­ ingeffec t onsoi lstructur e(Toutai n etal. , 1983),an dthroug hthei r burrowing activity (Jegen,1920 ;Kubiena ,1955 ;thi sthesis) ,thereb yinfluencin gaeratio nan d rootability ofth esoil . Inagricultura lfields ,thes eeffect s arepossibl ysmalle rtha n inmor enatura lhabitat s (Thompsone tal. , 1990),bu tfro mth epresen tstud y itap ­ pears,tha tthe yma yb equantitativel y importanto na fiel dscale . - Enchytraeid populations areinfluence d byvariou sagricultura l managementprac ­ tices,notabl ythroug heffect so namoun tan ddistributio no forgani c materiali nsoil . Itha srepeatedl y beenshow ntha tth equantit yan dqualit yo forgani cmatte rsup ­ pliedt oth esoi laffect s enchytraeid numbers,biomas san dactivit y (Sauerlandt& Marzusch-Trappmann, 1959; Kleyer &Babel ,1984 ;Lagerlö f &Andren ,1985 ; Nakamura,1988 ;thi sthesis) . Depthan dtyp eo ftillag einfluence sth evertica ldistributio n ofenchytraei dpopula ­ tionsan dhenc ethei ractivity ,throug hit sinfluenc eo nth edistributio n offres h organicmateria l (Ryl, 1977;Zimmermann ,1987 ;Lagerlö f etal. , 1989;thi sthesis) . Thetyp eo fcro pgrow nma yals ob eo fimportanc efo rth esiz ean dcompositio no f enchytraeidpopulation s inarabl efield s (Ryl, 1980;Lagerlö f etal. , 1989),roo t cropsbein g morefavourabl etha ncereal s (Ryl, 1980).

Seasonalfluctuation s inabundanc ean dactivit yar ea nimportan taspec to f enchytraeid effects onth efunctionin go farabl esystems . Fromth epresen tstud yi t appears,tha tmaximu mpopulatio nsize san dmaximu mactivit yoccu r insprin gan d earlysummer ,whe ncro pdemand sfo r nutrients usuallyar ehighest . Beneficialeffect s ofenchytraei d activitywil la ttha ttim econsis to fthei r influenceo nsoi lstructur ean d of theirindirec tpromotio no f nutrientmobilization . Onth eothe r hand,enchytraei dpopula ­ tionswil lconstitut ea ,b ei trathe rsmall ,poo lo f immobilized nutrients,i nth eorde ro f magnitudeo f 0.1g N/m 2. Thesenutrient swil lb erelease di nsumme ran dearl yau ­ tumn,whe npopulations ,bu tals oth enee dfo rnutrient so f mostcrops ,ar ediminishing . Assumingtha tenchytraei dtissue ,lik eearthwor mtissue ,i srapidl ydecompose dan d mineralized (Satchell,1967 ;Christensen ,1988) ,thi smigh timpl ya los so f nutrients

92 fromth esystem . Theus eo ffas tgrowin gcove rcrops ,a swa ssuggeste d byChris - tensen (1987)i nconnectio nwit hearthwor m populations,migh thel pt ocircumven tth e problemo fnutrien tlos si nthi speriod . Asecon dimportan tfeatur eo fth eeffect s ofenchytraei dactivit yi nagroecosys - tems,i sth evertica ldistributio no fth epopulations . Itma yb esupposed ,tha tadvanta ­ geouseffect s onnutrien tmobilizatio nan dsoi lstructur eevolutio nwil lb elargest ,an d chanceso fnutrien tlos sless ,whe nenchytraei dactivit yi sconcentrate di nth euppe rsoi l layers, wheremos to fth eroot sare . Thisi sth ecas ei nth eintegrate dfarmin gsyste m studied. Conversely,enchytraei dactivit yconcentratin g indeepe r layers,a si nth e conventionalfarmin gsyste mstudied ,ma yb edeeme dles sadvantageous ,becaus eo f thepresenc eo fles sroot sand ,therefore ,greate rchanc eo fleachin go fnutrients . Hence,enchytraeid s dopla ya nimportan tpar ti nth efunctionin g ofarabl esystem s intemperat eregions . Itwoul dsee mhowever ,tha tconcentratio no fenchytraei d activity inth euppe rlayer so fth esoi lprofil ei smor eadvantageous ,an dhelp st odiminis hth e risko f nutrientleachin gan dsoi lstructur edeterioration . Integratedagricultur ewil lbenefi tmos tfro mth eactivitie so fthes eanimals ,whe n management practicesinclud eshallo wtillage ,organi cfertilizatio nan dth eus eo fcove r crops.

93 8.Summar y

West-European contemporary ('conventional') agriculture ischaracterize d byhig h inputso fenerg yan dmatter ,an dha sle dt oseriou senvironmenta l problems,suc ha s pollutiono fwate ran datmosphere ,side-effect s ofpesticides ,an ddeterioratio n ofsoi l structure. Asa consequenc eo fthes eproblems ,ther ei sa nincreasin g interesti n ecologically soundagricultura lsystems ,i nwhic hmanagemen tpractice sar etune dt o botheconomi can denvironmenta l demands. Oneo fth eapproache s inthi srespect ,i s thedevelopmen t of'integrated 'agriculture ,characterize db ylowe rinput ,bu tmor e efficient use,o fenerg yan dmatter ,an db yyiel dreduction ,t ob ebalance d byth ereduc ­ tiono fcosts . Formor eefficien t useo fenerg yan dmatter ,a nimportan tpar ti st ob e playedb ybiologica lprocesse s insoil . Tomanag ethes eprocesse s properly,accurat e knowledgeo fth econtributio no forganism san dgroup so forganism st oth efunctionin g ofagroecosystem si sneeded . Thisthesi sdeal swit hth equestio no fth epar tplaye db y enchytraeids (Enchytraeidae,Oligochaeta ) inagroecosystems ,bot hi nth eflow so f energyan dmatter , andi nsoi lstructur eevolution . Theresearc hreporte dhere , was mainlyconducte do nvariou sdifferentl y managedfield so nth eexperimenta lfar m 'Dr. H.J.Lovinkhoeve ' inth eDutc h Noordoostpolder.

Thusfar , littlei sknow nabou tth epar tenchytraeid s playi necosystems ,bot h naturalan dmanaged . Acritica lrevie wo fth eecologica lliteratur eshowed ,that , al­ thoughi ti sclea rtha tenchytraeid s mustconstitut ea nimportan tfauna lgrou pi nth esoi l ofman yterrestria lecosystems ,thei r parti sdifficul tt oquantif y becauseo fscant y knowledgeo fth efactor s influencingpopulatio ndynamic s andactivity . Thisi sbecaus e moststudie s haveno tbee ncarrie dou ta tth especie s level,whil ei ti sclea rtha tther e existappreciabl einterspecifi c differences asregard sbiolog yan drespons et oenviron ­ mental factors.

Populationdynamics ,productio n ecologyan drol ei nnutrien tcyclin go f Enchytraeidaewer estudie ddurin gthre eyear s in four arablefield s atth e Lovinkhoeve experimentalsite . A'conventionally ' (withhig hinpu to fenerg yan dmatter ) managed fieldwa sstudied ,alon gwit hthre efield swit hvariou s'integrated '(wit h reducedinput ) managementtypes . Meanyearl yenchytraei dabundanc ean dbiomas si nthes esys ­ temsrange dfro m 11000ind/m 2 to4300 0ind/m 2an dfro m 0.08 gC/m 2t o0.4 2 g C/m2 respectively. Thedirec tcontributio no fenchytraeid s toth eflow so f energy andmatte r wascalculated ,base do nfiel ddat aan dparameter sfro mth eliterature . Inth e conven­ tionallymanage dfiel d 1.02 -2.58 %o fth eyearl yorgani ccarbo ninpu twa srespire db y theenchytraeids ,i nfield swit h integratedmanagemen tthi swa s0.5 2 -3.73% . Yearly nitrogenflu xfro mth epopulation s (throughstorag e inenchytraei dtissue ) wascalcu -

94 latedt orang efro m0.1 9t o0.6 0g/m 2. Theindirec tcontributio nt oth eflow s ofenerg y andmatter ,throug hth eeffect s ofenchytraei dactivit yo nothe rorganisms ,notabl y microorganisms,coul dno tb edetermined ,bu tma ywel lb e higher. Ingenera ln osignifican tdifference s inseasona ldynamics ,mea nabundanc ean d biomassbetwee nth einvestigate dfield swer efound . However,a pronounce ddiffer ­ encebetwee nth econventionall ymanage dfiel dan dth efield swit hintegrate dmanage ­ mentwa sfoun da sregard svertica ldistributio no fth eenchytraeids :i nth eintegrate d fieldsth epopulation swer emor econcentrate di nth esurfac elayers ,an di nth econven ­ tionalfiel dthe ywer emor eevenl ydistribute d indepth . Therear estron gindication stha t thevertica ldistributio nwa st oa larg eexten tinfluence db ysoi ltillag ean dth edistribu ­ tiono fenchytraeid s coincidedwit htha to forgani cfertilize ran dplan tresidues . Asa consequenceo fthi sdifferenc e invertica ldistribution ,ther ema yb ea greate r risko f leachingo fnutrient sfro ma conventionall ymanage dfiel da soppose dt ofield swit h integratedmanagement . Duringth egrowin gseason , theenchytraei ddistributio nwa sals oinfluence db yth e positiono fth ecro pplants ,indicatin ga nassociatio no fth eenchytraeid swit hroo texu ­ dates,eithe rdirectl yo rthroug hmicroorganisms .

Parto fth eresearc h reportedi nthi sthesi swa so fa fundamenta l nature,an dcon ­ cerneddeterminatio n of life-history parameterso fEnchytraeus buchholzi, themos t abundantspecie s atth eLovinkhoev eexperimenta lsite . Laboratoryexperiment swer e carriedout ,i nwhic hdevelopmen ttimes ,number so fcocoon s andegg sproduced , and longevitywer edetermine da tvariou stemperatures . Todetermin eth erelevanc eo f theseparameter sfo rprocesse soccurrin gunde rfiel dconditions ,populatio ndevelop ­ mentunde rmor enatura lcondition swa sals ostudied . Bya simpl esimulatio nmodel , thesedat pwer ecompare dwit hprediction sbase do nth elaborator ytrials . The com­ parisons/showed,tha tpopulatio ndevelopmen t underfiel dcondition s mayfal lshor tt o predictionsa sregard s abundance,bu to nth eothe rhand ,tha tindividua ldevelopmen t couldb eappreciabl yfaste rtha npredicted . Itseem sprobable ,tha tth ediscrepancie s foundar erelate dwit hth ephysiologica lconditio no fth eexperimenta lanimals ,an d that thelife-cycl ema yb eprolonge dunde runfavourabl econditions ,bu taccelerate dunde r favourableconditions .

Theresearc haddressin gth einfluenc eo fenchytraei dactivit yo nsoi lstructur e evolution,mad eus eo fdat afro mth epopulation-dynamica l study,an dfro ma fiel d experiment inwhic hartificia lsoi lcore swer eused ,wit hhighl yreproducibl esoi lphysica l characteristics. Inthi sthesis ,th emetho di sdescribe dt oproduc esuc hartificia lsoi l coresi nwhic hsoi lstructur ema yb emanipulate da sa variable . Thebasi cstep si nth e methodare : - homogenizationo fth esoi lb ysievin g - partialsterilizatio n byheating ,t oeliminat e metazoicanimal s

95 - compressiono fa predetermine damoun to fsoi lt oa certai n volume.

Thestructur ema yb eadjuste dt oth eneed so fa nexperimen t byvaryin gth emes h sizei nsievin go rth eamoun to fsoi lt ob ecompressed ,b yintroducin gartificia lmacro - pores,creatin gartificia lbarrier setc .

In thefiel dstud yo npopulatio ndynamic si twa sestablishe dtha t2 1- 35 %o fth e animalsi nth eenchytraei d populations carriedminera lgrain si nth edigestiv etract . The calculatedtranspor to fminera lmateria li nth euppe r0. 4m amounte dt o0.00 1- 0.0 1% ofth ebul ksoi lpe ryear . Fromthis ,i tma yb econclude dtha tactiv eburrowin gb y enchytraeids isquantitativel yo f minorimportance . Fromth efiel dexperiment ,however ,a nappreciabl eeffec to fenchytraei d activity onsoi lstructur eappeared :i nexperimenta lcore sfro m Lovinkhoeve soil,wit h enchytraeids present,th eai rpermeability ,th evolum eo fpore si nth esiz eclas scorre ­ spondingt oenchytraei d bodywidth ,an dth eproportio n ofaggregate scorrespondin gt o thesiz eo fthei rfeca lpellet swer ehighe rtha ni ncore swithou tenchytraeids . Thiseffec t mayb eexplaine db yth eremova lo fpor eneck sdurin gburrowing ,an db yth etranspor t oforgani cbeside s mineralmaterial . Thishypothesi si scurrentl y beingtested ,usin g polished blocksfro mth eartificia lsoi lcores .

Generalconclusion s canb esummarize d asfollows :

- Directcontributio no fenchytraeid s(throug hthei rmetabolism ) toth eflow so fen ­ ergyan dnutrient si nagroecosystem si si nth eorde ro f magnitudeo f 1% ,an di s similart otha ti nmor enatura lhabitats . Indirecteffect s (notablythroug hthei r influenceo nmicrobia lactivity ) mayb emuc hhigher . - Theevolutio no fsoi lstructur ei saffecte d byenchytraeid si nsevera lways :throug h theproductio no fexcrement san dmucilage stha t mayhav ea stabilizin g effecto n soilstructure ,an dthroug hthei r (selective) burrowingactivity ,thereb yinfluencin g aerationan drootabilit yo fth esoil . - Enchytraeidpopulation s areinfluence d byvariou sagricultura lmanagemen tprac ­ tices,notabl ythroug heffect so namoun tan ddistributio no forgani cmateria li nsoil . Thus,dept han dtyp eo ftillag einfluence sth evertica ldistributio no f enchytraeid populationsan dhenc eo fthei ractivity . Thetyp eo fcro pgrow nma yals ob e of importancefo rth esiz ean dcompositio no fenchytraei dpopulation s inarabl efields .

Seasonalfluctuation s inabundanc ean dactivit yar ea nimportan taspec to f enchytraeid effectso nth efunctionin go farabl esystems . Fromth eresearc h presented inthi sthesi si tappears ,tha tmaximu mpopulatio nsize san dmaximu mactivit yalmos t completely coincidewit hth eperio do fmaximu mcro pgrowth ,whe ncro pdemand sfo r nutrientsusuall yar ehighest . Beneficialeffect so fenchytraei dactivit ywil la ttha ttim e

96 consisti nthei r influenceo nsoi lstructur ean di nthei rindirec tpromotio no fnutrien t mobilization. Nutrientsstore di nenchytraei dtissu ewil lmainl yb erelease d insumme r andearl yautumn ,whe n populations,bu tals oth enee dfo rnutrient so f mostcrops ,ar e diminishing. Theris ko f losso f nutrientsfro mth esystem ,notabl y inconventionall y managedfields ,ma yb ecounteracte d byth eus eo ffas tgrowin gcove rcrops . Ecologicallysoun dagricultur ewil ltherefor ebenefi tmos tfro mth eactivitie so f theseanimals ,whe nmanagemen tpractice s includeshallo wtillage ,organi cfertilizatio n andth eus eo fcove rcrops .

97 9.Samenvattin g

Dei nWest-Europ agangbar e('conventionele' ) landbouwmethodes wordengeken ­ merktdoo ree nhog einpu tva nenergi ee ngrondstoffen ,e nblijke naanleidin gt egeve n toternstig emilieuproblemen ,zoal svervuilin gva nwate re natmosfeer , neveneffecten vanbestrijdingsmiddele n enverslechterin gva nd ebodemstructuur . Tegend eachter ­ grondva ndez eprobleme nbestaa te ree ntoenemend ebelangstellin gvoo roecologisc h verantwoorde landbouw,waa ri nd ebeheersmaatregele n zowelme teconomisch eal s metmilieu-eise nrekenin gword tgehouden . Een vand ebenaderinge n hierbiji she t strevennaa r'geïntegreerde 'landbouw ,gekenmerk tdoo rminde rinput ,maa refficiënte r gebruik,va nenergi ee ngrondstoffen ,e ndoo ree nlager eopbrengst ,di eword tgecom ­ penseerddoo rlager ekosten . Voordi tefficiënte r gebruikva nenergi ee ngrondstoffe n isee nbelangrijker e rolweggeleg dvoo rbiologisch eprocesse n ind ebodem . Om zo goedmogelij kva ndez eprocesse n gebruikt ekunne nmaken ,i skenni svereis tva nd e bijdrageva norganisme ne ngroepe nva norganisme naa nhe tfunctionere nva nland - bouwsystemen. Indi tproefschrif tstaa td evraa gcentraa l naard ero lva npotworme n (Enchytraeidae,Oligochaeta ) inagro-oecosystemen ,zowe lwa tbetref t deenergie -e n stofstromendi ehie roptreden ,al swa tbetref t hunro li nd eontwikkelin gva nd ebodem ­ structuur. Hetonderzoe kwaarva n hierversla gword tuitgebrach t concentreerde zicho p enkeleverschillen d beheerde akkerso pd eDr .H.J . Lovinkhoevei nd eNoordoost ­ polder.

Watbetref t potwormeni sno gmaa rweini gbeken dove rhu nro li noecosystemen , zoweli nnatuurlijk eal sagro-oecosystemen . Eenkritisc honderzoe kva nd eoecologi - scheliteratuu r ophe tgebie dva npotworme n leerde,da tenerzijd sduidelij k isda tpot ­ wormeni nvee lterrestrisch eoecosysteme nee nbelangrijk egroe pva nd ebodemfaun a moetenvormen ,anderzijd shu nro lmoeilij kt ekwantificere n is,omda ti nd emeest e gevallengee nduidelijkhei d bestaatove rd efactore ndi eee nro lspele nbi jhu n aantal­ sontwikkeling enactiviteit . Ditkom tvoor t uithe tfei tda ti nd emeest egevalle ngee n onderzoek opsoortsnivea uheef tplaatsgevonden ,terwij ltegelijkertij d duidelijk is,da te r aanzienlijkeverschille n bestaantusse nsoorte nwa tbetref t hunbiologi ee nhu nreacti e opomgevingsfactoren .

Onderzoek aand epopulatiedynamie kva npotwormen ,hu nproductie-oecologi ee n hunro li nd estofkringlope nwer dgedurend edri ejaa ruitgevoer do pvie r akkerso p de Lovinkhoeve. Hierwer dee n'conventioneel '(me thog einpu tva nenergi ee ngrondstof ­ fen) beheerdeakke r bestudeerd,naas to pverschillend e manieren 'geïntegreerd'(me t verminderde input) beheerdeakkers . Degemiddeld ejaarlijks edichthei d enbiomass a vanpotworme ni ndez esysteme nvarieerde nrespectievelij kva n1100 0ind/m 2to t

98 43000ind/m 2,e nva n0.0 8 gC/m 2to t0.4 2 gC/m 2. Dedirect e bijdrageva npotworme n aand eenergie -e nstofstrome nwer dbereken do pbasi sva nd eveldwaarneminge ne n parameters uitd eliteratuur . Ind e'conventioneel 'beheerd eakke rwer d1.0 2- 2.58% vand ejaarlijks e inputaa norganisch e koolstof doord epotwormpopulatie sverademd ; ind e'geïntegreerde 'akker swa sdi t0.5 2- 3.73% . Tevenswer dbereken dda td e hoeveelheidstiksto f diejaarlijks ,vi aopsla gi npotwormweefsel ,d epopulatie sverliet , varieerdeva n0.1 9to t0.6 0g/m 2. Hunindirect ebijdrag eaa nd eenergie -e n stof­ stromen,vi ad einvloe do phe tfunctionere nva nander eorganismen ,me tnam ebac ­ teriëne nschimmels ,ko nnie tworde nbepaald ,maa rhe tlijk twaarschijnlij k datdez e hogerligt . Watbetref tseizoensdynamie ke ngemiddeld eaantalle ne nbiomass awerde ne r overhe talgemee ngee nduidelijk everschille ngeconstateer dtusse nd eonderzocht e akkers. Welwa se ree nonmiskenbaa rverschi li nd evertical everdelin gva nd epot ­ wormpopulaties tussend econventionee lbeheerd eakke re nd eakker sme tgeïnte ­ greerdbeheer :i nd egeïntegreer d beheerdeakker skwame nd epopulatie s meervoo ri n deoppervlakkig e lagen,i nd econventionee l beheerdeakker s meergelijkmati gver ­ spreidove rhe tprofiel . Ditverschi li nvertical everdelin ghin gwaarschijnlij k samenme t verschilleni ngrondbewerkin g end eresulterend everdelin gva ngewasreste n en organ­ ischemest . Eenmogelij kgevol gva ndi tverschi l invertical everdelin g is,da td ekan s opverlie sva nnutriënte ndoo ruitspoelin ggrote ri si nee nconventioneel ,da ni nee n geïntegreerdbeheerd eakker . Gedurende hetgroeiseizoe nwer dteven see npositiev erelati egeconstateer d tussend ehorizontal everdelin gva nd epotworme n end epositi eva nd e gewasplanten. Ditwijs to pee nassociati eva npotworme nme twortelexudaten ,hetzi jrechtstreeks , hetzijvi ad ehie rvoorkomend emicro-organismen .

Eendee lva nhe ti ndi tproefschrif t besproken onderzoekwa sva nfundamentee l biologischeaard ,e nbetro f hetvaststelle nva nlife-histor yparameter sva n Enchytraeus buchholzi, demees tvoorkomend esoor to pd eLovinkhoeve . Hiervoorwerde ni nhe t laboratorium experimenten uitgevoerd, waarinontwikkelingstijden ,aantalle ncocon se n eierenpe rindividu ,e nd elevensduu r bijverschillend etemperature nwerde nbepaald . Omd ewaard eva ndez egegeven svoo rd eonde rveldomstandighede noptredend e processent ebepalen , werdteven sd epopulatieontwikkelin g ondermee rnatuurlijk e omstandigheden bepaald. Metbehul pva nee neenvoudi gsimulatiemode lwerde ndez e gegevensvergeleke n metd evoorspellinge n opbasi sva nd elaboratoriumexperimen ­ ten. Hieruit kwamnaa rvoren ,da tenerzijd sd epopulatieontwikkelin g onderveldom ­ standighedenwa tbetref taantalle nko nachterblijve n bijd evoorspeld ewaarden ,maa r anderzijdsd eindividuel e ontwikkelingaanzienlij k snellerko nverlope nda n voorspeld. Hetlijk twaarschijnlijk , datd egevonde ndiscrepanti esamenhang t metd efysiologisch e conditieva nd eproefdieren ,waarbi ji nongunstig eomstandighede n delevenscyclu s kanworde nverleng de ni ngunstig ejuis tverkort .

99 Voorhe tonderzoe knaa rd eeffecte nva npotwormactivitei t opd eontwikkelin gva n debodemstructuu rwer dgebrui kgemaak tva ngegeven sui td epopulatiedynamisch e studiee nui tee nveldexperimen t metkunstmatig ebodem sme ti nhog emat erepro ­ duceerbarebodemfysisch eeigenschappen . Indi tproefschrif tword td emethod e beschreveno mdergelijk ekunstmatig ebodems , waarind ebodemstructuu r alsvari ­ abelegemanipuleer d kanworden ,t evervaardigen . Debelangrijkst e stappeni nhe t proceszijn : - homogeniserenva nd egron ddoo rzeve n - gedeeltelijke sterilisatieva nd egron ddoo rverwarming ,waardoo rd eaanwezig e meercelligediere ngedoo d worden. - samenpersenva nee nvastgesteld e hoeveelheidgron dto tee nbepaal dvolume .

Manipulatieva nd estructuu rva ndergelijk ekunstmatig ebodem ska ngebeure n doorvariatie si nd emaaswijdt ebi jhe tzeve no fi nd erelatiev ehoeveelhei dsame nt e persengrond ,doo rhe taanbrenge nva n kunstmatige macroporiëno f hindernissenetc .

Tijdens hetpopulatiedynamisc honderzoe kwer dbi j2 1- 35 % vand ediere ni nd e potwormpopulatiesmineral edeeltje s inhe tspijsverteringskanaa l aangetroffen. Op basishierva nwer dbereken dda the tjaarlijks etranspor tva nmineral edeeltje s opdez e manier0.00 1- 0.0 1% bedroegva nhe tbodemvolum e ind ebovenst e0. 4 mva nhe t profiel. Hieruitka ngeconcludeer dworden ,da tactie fgrave ndoo rpotworme n kwantita­ tief vanondergeschik t belangis . Inhe tveldexperimen t kwamechte ree naantoonbar einvloe dva n potwormactiviteit opd ebodemstructuu r naarvoren :i nkunstmatig ebodem sva ngron dva nd eLovink - hoeve,waari npotworme naanwezi gwaren ,ware nd eluchtdoorlatendheid ,he tpo ­ riënvolumei nd egrootteklass edi ecorrespondeer t metd edikt eva npotwormen ,e nhe t aandeelva naggregate n ind egrootteklass eva npotwormexcremente ngrote rda n in bodemszonde rpotwormen . Diteffec t kanverklaar dworden ,doo raa nt eneme nda td e graafactiviteitva npotworme nvoora loptreed tbi jvernauwinge n inporiën ,e nda t be­ halvetranspor tva nmineraa lmateriaal ,oo korganisc hmateriaa lword tgetransporteerd . Dezehypothes eword tn ugetoets taa nd ehan dva npolijstblokke n dieva nd ekunstma ­ tigebodem szij ngemaakt .

Dealgemen econclusie skunne nal svolg tworde nsamengevat : - Dedirect e bijdrage (viahu nmetabolisme ) vanpotworme naa nd estrome nva n energiee nnutriënte n inagro-oecosysteme nlig ti nd eord eva ngroott eva n 1% , eenwaard edi evergelijkbaa r isme tdi ei nmee rnatuurlijk e systemen. Indirect, metnam evi ahu ninvloe do pmicrobiël eactiviteit ,ka nhu nbijdrag eechte rvee l groterzijn . - Deontwikkelin gva nd ebodemstructuu rword tdoo rpotworme no pverschillend e manieren beïnvloed:doo rd eproducti eva nexcremente ne nslij mka nd estruc -

100 tuurstabiliteitbevorder dworden ,e ndoo rhu n(selectieve ) graafactiviteithebbe nzi j effecto pd ebeluchtin ge nbewortelbaarhei dva nd e grond. - Potwormpopulatiesworde nbeïnvloe ddoo rhe tlandbouwkundi g beheer,me tnam e waarda teffec t heefto pd ehoeveelhei dorganisch esto f ind ebodem ,e nd everde ­ lingdaarvan . Devertical everdelin gva npotworme nove rhe tprofie lword t zodoende beïnvloed doord evor mva ngrondbewerkin g dieword ttoegepast . Ook hetsoor tgewa swa tword tgeteel dzo uva nbelan gkunne nzij nvoo rd eontwikke ­ linge nactivitei tva npotwormpopulaties .

Eenbelangrij kaspec tva nd ero lva npotworme ni nhe tfunctionere nva nland - bouwsystemeni sd eseizoensdynamie ki naantalle ne nactiviteit . Inhe ti ndi t proefschrift beschrevenonderzoe kviele nd emaximu mpopulatiegrootte s en-activitei t vrijwelsame nme td eperiod eva nd egrootst egewasgroei ,wannee r debehoeft eva n hetgewa saa nnutriënte n hetgroots t is. Dithoud ti nda tee ngunstig e invloedva n potwormeni ndi etij dvoora lzo ubestaa ni nhu ninvloe do pstructuurvormin g enhu n indirecteeffecte n opd emobilisati eva nnutriënten . Dei nd epotwormpopulatie szel f opgeslagen nutriënten komenvoora lvri jgedurend ed ezome re nhe tbegi nva nd e herfst,wannee rd epopulatie safnemen ,evenal sd ebehoeft eaa nnutriënte nva nd e meestegewassen . Hetmogelijk everlie sdoo ruitspoelin gwa thiervan ,voora li n'con ­ ventioneel' beheerdeakkers ,he tgevol gka nzijn ,ka nworde ntegengegaa ndoo rge ­ bruikt emake nva nee nsnelgroeien dtussengewas . Inoecologisc hverantwoord e landbouwsystemenka nda noo khe tbest egebrui k wordengemaak tva nd eactivitei tva ndez ediergroe pdoo rhe ttoepasse nva nondiep e grondbewerking,organisch ebemesting ,e n tussenteelten.

101 10.Reference s

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116 Curriculum vitae

WimDidde nwer dgebore no p4 decembe r 1950i nWaalwijk . In197 0 be­ haaldehi jhe tdiplom aGymnasium- ß aanhe tDr .Mollercolleg et eWaalwijk . Daarnastudeerd ehi jbiologi ee nwijsbegeert eaa nd eRijksuniversitei t Utrecht,e nbewerkt ei nd edoctoraalfas evakke ni nvegetatiekunde ,biologi e ensamenleving ,toegepast ezoölogisch eoecologie ,e nnatuurbehee re n natuurbehoud. In juni 1977studeerd ehi ja fal salgemee nbioloog . Totme i197 9vervuld e hijvervolgen szij nvervangend edienstplich t bijd e afdelingBotani eva nhe tRijksinstituu tvoo rNatuurbehee r inLeersum . Van 1984to t198 6wa shi jachtereenvolgen swerkzaa mbi jd evakgroepe n Dieroecologie enNematologi eva nd eLandbouwuniversiteit , waarhi jonde r andereee nstudi everrichtt enaa rd einvloe dva nd ebodemstructuu r opd e verspreidingva nspringstaarten . Vanafjanuar i 1986i shi jverbonde n aand evakgroe p Bodemkundee n Geolo­ gieva nd eLandbouwuniversiteit ;to tapri l 1989al spromotieassistent ,daarn a alsuniversitai r docentbodembiologie .