HENK SIEPEL

STRUCTURE AND FUNCTION

OF

SOIL MICROARTHROPOD COMMUNITIES

CENTRALE LANDBOUWCATALOGUS

0000 0572 1341 Promotor: Dr. L. Brussaard Hoogleraar ind e Bodembiologie AlfJOï'të"J*P >o J /OcgZ^

HENK SIEPEL

STRUCTURE AND FUNCTION

OF

SOIL MICROARTHROPOD COMMUNITIES

Proefschrift terverkrijgin g van de graad van doctor ind e landbouw- en milieuwetenschappen op gezagva n de rector magnificus, dr. C.M. Karssen, inhe t openbaar te verdedigen op dinsdag 20 september 1994 des namiddags tehal f twee ind e Aula van de Landbouwuniversiteit teWageningen . CIP-DATAKONINKLIJK E BIBLIOTHEEK, DEN HAAG

Siepel, Henk

Structure and function of soilmicroarthropo d communities / Henk Siepel. -[S.I.:s.n.]

Thesis Wageningen. -Wit h réf.- With summary inDutch . ISBN 90-9007450-3 NUGI 825 Subject headings: soilbiolog y / ecotoxicology /natur e management

The investigations described in this thesis were carried out at the Department of Animal Ecology of the DLO- Institute for Forestry and Nature Research (IBN-DLO), The Netherlands

;•;_',.; -."IVEKS l STELLINGEN

behorende bijhe tproefschrif tva nHen kSiepel : Structure and function of soil microarthropod communities

1. Foresie isgee nr-geselecteer dkenmerk ;he t isee nmanie rva nvervoe r tussengeschikt e biotopen die inoverigen s ongeschikt terreinliggen . (Dit proefschrift, Binns E.S. 1982, Biol Rev: 57, 571-620)

2. Hetgebrui kva nzic hasexuee lreproducerend e dieren inoecotoxicolo - gische toetsengeef t geenrepresentatiev e resultatenvoo rd esoort , laat staanvoo rgroepe nva nsoorten . (Dit proefschrift)

3. Hetactuel egebrui kva nvoedingsmogelijkhede ngeef tallee n inzicht in deautoecologi e vanee nsoor t invergelijkin g methe tpotentiee laa n voedingsmogelijkheden. (Dit proefschrift)

4. Demat eva n chitinaseactiviteit ind epopulatie sva nmicroarthropode - soorten indiceert demat eva nongestoordhei dva nhe t afbraakproces vanorganisc hmateriaa l opzwa kzur ebodems . (Dit proefschrift)

5. Bij lagemobilitei t kunnenmee r soorten samenvoorkome n danda te r bronnenva nbestaa nzijn . (Dit proefschrift, n.a.v. Arthur W. 1987, The niche in competition and evolution, Wiley & Sons, Chichester, UK)

6. Uitsluiting door concurrentie iszeldzaam . (Dit proefschrift, Hardin G. 1960, Science 131: 1292-1297)

7. Begrazingva nnatuurterreine n dientvoornamelij k omt e latenzie nda t het terreinbeheer dwordt ;d evermeen d gunstige effecteno pd enatuu r zijnnooi tbewezen .

8. Onderzoeknaa r dosis-effect relaties ind eoecotoxicologi e heeft geen betekenis alshe tnie tgekoppel dword tme tautoecologisch e en systeemoecologischekennis .

9. Oecologenonderschatte n denatuurwaarde nva nhe t stedelijke n landelijkgebied .

10. Indicatorenvoo rbiodiversitei t zijnee ncontradicti o interminis .

11. Vergrotingva n deonvoorspelbaarhei d vanhe tmilie ubevorder tbehalv e demobilitei tva n deén egroe pvoora loo khe tuitsterve nva nander e groepen.

12. Onderzoeknaa rnatuurontwikkelin gword t zeldenvana fd ebode m opgebouwd.

Wageningen,2 0septembe r 1994 Voor mijn ouders Contents

Contents

Abstract 7 Voorwoord 9 1. General introduction 11 2. Life-history tactics ofsoi l microarthropods 15 (Biology and Fertility of Soils, in press) 3. Applications ofmicroarthropo d life-history tactics innatur e management andecotoxicolog y 51 (Biology and Fertility of soils, in press) 4. Feeding guilds oforibati d mites basedo nthei r carbohydrase activities (with Elze deRuiter-Dijkman ) 69 (Soil Biology and Biochemistry 25 (1993), 1491-1497) 5. Mites ofdifferen t feeding guilds affect decompo­ sitiono forgani c matter (with Frans Maaskamp) 81 (Soil Biology and Biochemistry, in press) 6. Coexistence insoi l microarthropods 95 (subm.) 7. Competitive exclusion isno ta genera l ecological principle 117 (subm.) 8. General discussion 121 Summary 131 Samenvatting 133 Curriculum vitae 136 Abstract

Abstract

Microarthropod species were classified according to life-history tactics and feeding guilds. Twelve life-history tactics were distinguished, based on well-defined life-history traits like the type of reproduction (thelytoky, arrhenotoky, sexual reproduction), oviposition (semelparity, iteroparity), development, synchronization (of the life cycle with en­ vironmental conditions), and dispersal (phoresy, anemochory). Examples are given of the distribution of these tactics among microarthropod species occurring in several biotopes, during decomposition of organic matter, and under several types of disturbance and pollution. Thelyto- kously reproducing species appeared tohav e higher numbers at sites with a persistent pollution. Feeding guilds were defined on the basis of gut carbohydrase (cellu- lase, chitinase, and trehalase) activities. Five species-rich guilds were recognized. In the presence of species able to digest the fungal cell-wall next to cell-contents (called fungivorous and herbo-fungi- vorous grazers), a higher C02 evolution during decomposition of pul­ verized litter was found than in their absence. In the presence of species able to digest cell-contents only (called fungivorous browsers and opportunistic herbofungivores), in such experiments a lower C02 evolution was found than in their absence. In a simulation model it was tested whether relatively inefficient use of food may be compensated by life-history traits or abilities by which short-term environmental extremes canb e overcome. Having the pos­ sibility to bridge a relatively long period of food shortage, or withstanding extremes in drought, frost or heat, or having a higher mobility, was indeed shown to result in a better survival of species that use their food relatively inefficiently. This results in the effect that species with different life-history tactics can coexist on the same food sources. Contradictory to the principle of competitive exclusion, species with identical niches may coexist when the mobility of these species isno t unlimited.

Key-words: Acari, Collembola, Life-history, Feeding guild, Coexistence, Decomposition, Nature management, Ecotoxicology. Voorwoord

Voorwoord

Hoewel ik al heel jong belangstelling had voor biologie en van alles liep te bekijken als mijn vader en opa aan het vissen waren, had ik nooit gedacht dat ik me met mijten en springstaarten bezig zou houden. Voor ik in oktober 1984 op het toenmalige Rijksinstituut voor Natuur­ beheer kwam, wist ik net dat mijten acht poten hebben (met uitzondering van de larfjes) en springstaartjes zes. In het onderzoek op graslanden naar indicatorsoorten en evaluatiemethoden, waar ik me op moest gaan richten, waren dit ook al geen voor de hand liggende groepen. Bij mijn aanstelling werd ik echter geconfronteerd met enige nog uit te werken datasets van deze microarthropoden. Deze datasets waren toch verzameld inhe t kader van het monitoringonderzoek op graslanden omdat ze volgens Chris van de Bund heel precies de toestand van het grasland aangaven. Chris bracht dit zo overtuigend en stimulerend dat ik niet alleen de datasets uitwerkte en eenbemonsterin g vanmicroarthropode n inhe t gras- landenonderzoek opnam, maar uiteindelijk zelf ook naar de mijten en springstaarten ging kijken. In de loop van het onderzoek bleken inder­ daad heel goede indicatoren te vinden onder de microarthropoden, maar dat gold ook voor de grotere insekten en spinnen, die voor eenpraktijk ­ toepassing devoorkeu r kregen. Maar de teerling was geworpen en ik was geïntrigeerd geraakt door de wereld onder het bodemoppervlak. De talrijkheid van de beestjes, hun soortenrijkdom, hun veelheid aan vormen, ook in ecologisch opzicht, maakten dat ikm e nog gauw door Chris liet inwijden ind e herkenning van microarthropoden voor Chris in 1987 de dienst verliet en ik formeel op zijn plaats kwam. Overigens bleef Chris ook daarna bereid de determina­ tieva n soorten die ikvoo r het eerst zag teverifiëre n en geen idee was te wild om er eens serieus over door te bomen. Ook de anderen die als klankbord hebben gediend binnen en buiten het maandelijks entomologen- overleg op het instituut wil ik bedanken voor hun opbouwend commentaar, hun suggesties en het critisch doorlezen van de concepten, met name Frits Bink, Walter van Wingerden, Mari Verstegen, Rob Hengeveld, en bij het modelwerk Hilko van der Voet en Rienk-Jan Bijlsma. Enkele belang­ rijke hoofdstukken van dit proefschrift waren er misschien nooit gekomen zonder de hulp en inzet van Elze de Ruiter en Frans Maaskamp. Ruut Wegman wil ik graag bedanken voor het tekenen van de figuren. Prof. dr. Lijbert Brussaard wil ik bedanken dat hij als promotor op wil treden en voor zijn inspirerend enthousiasme waarmee hij de concepten te lijf ging en van critisch commentaar voorzag, zodat ze ook voor niet direct be­ trokkenen leesbaar werden. Furthermore I like to thank Prof. dr. M.B. Usher, who strengthened me in my view that identifications in soil microarthropods should go to the species level as he stated in the Voorwoord meeting of soil biologists of the Nordic Ecological Society in Denmark. I am glad that he instantly affirmatory responded to my invitation for the graduation committee. Rest mij nog een woord van dank aan het thuisfront, Annet, Anika en Hanneke, geen oase van rust, maar wel een heel andere wereld om in te vertoeven na dagenva nmijten , analyses en computers. Het overwerk ind e avonduren zal wel niet helemaal afgelopen zijn, maar wordt hoop ik wel minder nu het proefschrift afgerond is. Pa en ma bedankt voor de niet aflatende steun en devel e oppasdagen.

Arnhem, 11jul i 1994 w

10 General introduction

The soil fauna isver y rich inspecies ;protozoans ,nematodes , arthropods and annelids are the major groups of animals,bot h innumbe r of species, andi nbiomass .Thi sthesi swil lfocu so nth esoi larthropods ,particularl y the microarthropods, the group most rich in species. All soil mites (Acari), andprimar ywingles s insects,predominantl y springtails (Collem- bola)ar e includedi nth esoi lmicroarthropods .Mite sar ea subclas so fth e spiders, which in The Netherlands contains six orders: Metastigmata (ticks),Oribatid a (mossmites) ,Acaridida ,Mesostigmat a(predator ymites) , Actinedida (spidermites ,harves tmites ,wate rmites ,etc. )an dTarsonemid a (with the Actinedida also called Prostigmata). Next to these commonly acceptedname sman ysynonym sar euse d (Vande rHamme n1972 ).Oribati dmite s are the most abundant in forest soils, followed by Collembola and Mesostigmata. Actinedida and Tarsonemida are sometimes very abundant in grassland and arable soils.Acaridid a formmos t of the time aminorit y in numbers inth esoi lfauna .Wit hrespec tt ospecie srichnes s inth esoi lth e Actinedida are the first inrank ,bu tman y species live in the vegetation andar efoun di nsoi lsample sonl yaccidentally .Oribatid aar enex ti nran k inspecie srichness ,followe db yMesostigmata ,Collembola ,Tarsonemida ,an d Acaridida. Species richness isthough t tob erelate d tosurface :th e largera sit e the more species can be present (MacArthur & Wilson 1967). The highest species richness among oribatids varies from on average 33 oribatid mite speciespe r50 0cm 2 (range23-45 )i nCentra lEuropea nforest s (Moritz 1965) to4 5oribati d speciespe r 250cm 2 (range 37-52)i nunmanage dDutc hgrass ­ lands (Siepel& Va nd eBun d 1988).Karppine n (1958)foun da naverag e of1 9 oribatid mite species (range 8-26) per 5 cm2 in Finnish forests. Species richness for all microarthropods together is even much higher, up to 108 species per 500 cm2 (Siepel & Van de Bund 1988). Assumin g that every speciesha sa nuniqu eniche ,accordin gt oth ehypervolum emode l (Hutchinson

11 Microarthropod communities

1957), an d that competitive exclusion leads to minimizing niche overlap (Hardin 1960), one must conclude that in the soil a tremendous variation in resources has to exist (Anderson 1975). Theoretically this may be possible,bu t are the animal species able todistinguis h and select those resources? The alternative solution is thatdifferen t speciesma y use the same resources (food, shelter, etc.) without mutual exclusion. A less efficientus e of resources mightb e compensatedb y certainadaptation s in the life-history. The objective ofthi sthesi s ist oinvestigat ewhethe r alimite dnumbe r of resources allows the coexistence of a higher number of species. This question requires operational knowledge about the structure and function of soil microarthropod communities. The structure is explained from dif­ ferences in life-history tactics resulting in different abilities to overcome suddenhars h environmental conditions.Th e function is explained fromdifferen tfeedin gguild so fmicroarthropods .Thes eguild sar edefine d onth ebasi s of activities ofcarbohydras e gut enzymes.Th e differentef ­ fectsrepresentative s ofthes e feedingguild shav e onth erat eo fdecompo ­ sition of organic matter may be explained from differences in digestion capacities.

Inchapte r 2 the life-history traits of soilmicroarthropod s are dealt with to present a solid base for the definition of life-history tactics. Several life-history traitspas s inrevie wan dth eecologica l significance of thelytoky, either automictic orapomictic ,arrhenotoky , amphitoky,an d sexualreproductio nar eexplained .A classificatio no ftwelv e life-history tactics,base do nwell-defined ,underive d traits ispresente dan dcompare d with the classifications ofMacArthu r andWilso n (1967), Grim e (1977)an d Southwood (1977) and with the multidimensional classification of Stearns (1976). For every tactic the functional relation with the most important biotopes isdescribed . Examples of species from each systematic order are givenwhe n available. In chapter 3 a key is presented as a tool for the identification of life-history tactics. Examples of the distributions of microarthropod species among life-history tactics are presented for the soil fauna of a forest, a grassland, and a saltmarsh. The practical applicability of the defined life-history tactics is subsequently illustrated in nature management and ecotoxicology. The common use of asexually reproducing species in ecotoxicology is discussed. Inchapte r4 forty-nin eoribati dmite san don eacaridi dmit ear eclassi ­ fied in feeding guilds based on their gut carbohydrase activities. Three carbohydrases were selected to differentiate between food sources. Cellulaseactivit y indicatesdigestio no fplan tmaterial ,includin galgae , trehalase activity indicates digestion of the cell-contents of fungi,

12 General introduction lichens, andblue-gree n algae,an dchitinas e activity indicates that also the fungal cell-walls can be digested. Herbivorous grazers, herbivorous browsers, fungivorous grazers, fungivorous browsers, herbofungivorous grazers, opportunistic herbo-fungivores, and omnivores are proposed as feeding guilds, with grazers able to digest most of the ingested food components, andbrowser s able to digest the cell-contents only. In chapter 5 the decomposition of litter by fungi in thepresenc e and theabsenc eo frepresentative so fth efiv emajo rfeedin gguild si sstudied . The implications of the new classification of feeding guilds for insight into the role of mites in the decomposition of organic matter are discussed. Differences inefficienc y of food-processing may result ina selective advantage of themor e efficient mites. Inchapte r 6a simulatio n model is presented toevaluat epossibl eway so fcompensatio n forth eles sefficien t mites by differences in life-history tactics,mobility , or tolerance for short-term extreme conditions (drought, frost,heat , food shortage). Chapter 7deal swit ha specia lapplicatio no fth esimulatio nmodel :th e test of the 'principle of competitive exclusion' (Hardin 1960). In the simulation model two species are defined as identical. In a first set of runsbot h specieshav en orestriction s inmobilit y (asi na Lotka-Volterr a model) and in a second set of runs both species are restricted in their mobility (asusuall y innature) . Thepossibl e co-occurrence of 'identical species' is discussed and related to speciation rates. In the general discussion (chapter 8) the approach followed in this thesisan dth eresult sobtaine dar eevaluated .Th etrait sa specie sca nus e tosurvive ,eithe rlife-histor ytraits, digestio ncapacities ,o rpossibili ­ ties to overcome short-term extreme conditions, determine the potential range ofbiotope s that species can inhabit.Thi sma yb e abette r starting pointfo rth ecoexistenc eo fspecie sunderstandin g insoi ltha ncomparison s of species communities and microhabitat characteristics.

REFERENCES

Anderson, J.M., 1975. The enigma of soil animal species diversity. In: Vanek,J . (ed.)Progres s insoi lzoology ,Jun kBV ,De nHaag ,pp .51-58 . Grime,J.P. , 1977.Evidenc e for the existence of threeprimar y strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169-1194. Hardin, G., I960. The competitive exclusionprinciple . Science 131,1292 - 1297. Hutchinson, G.E., 1957. Concluding remarks. Cold Spring Harbour Symposia in quantitive biology 22,415-427 .

13 Microarthropod communities

Karppinen,E. ,1958 .Übe rdi eOribatide n (Acar.)de rfinnische nWaldböden . Annales Zoologici Societas ZoologiesBotanie sFennica e 'Vanamo' 19(1), 1-43. MacArthur, R.H. & E.O. Wilson, 1967. The theory of island biogeography. Princeton University Press,Princeton , N.J. Moritz,M. , 1965.Untersuchunge nübe r denEinflu ßvo n Kahlschlagmaßnahmen aufdi eZusammensetzun gvo nHornmilbengemeinschafte n (Acari:Oribatei ) norddeutscher Laub- und Kiefernmischwälder. Pedobiologia 5, 65-101. Siepel,H .& Va nd eBund ,CF. , 1988.Th einfluenc eo fmanagemen tpractice s onth emicroarthropo dcommunit yo fgrassland .Pedobiologi a31 ,339-354 . Southwood, T.R.E., 1977.Habitat , the templet for ecological strategies? Journal ofAnima l Ecology 46,337-365 . Stearns, S.C., 1976. Life-history tactics: a review of the ideas. Quarterly Review Biology 51,3-47 . Van derHammen ,L. ,1972 .Spinachtigen ,Arachnoidea . IV.Mijten ,Acarida . Algemene inleiding in de acarologie. Koninklijke Nederlandse Natuur­ historischeVereniging ,Wetenschappelijk eMededelin g 91.Hoogwoud ,Th e Netherlands.

14 Life-history tactics of soil microarthropods

SUMMARY. Inorde r toprovid e asoun dbasi s for defining life-history tac­ tics,severa l life-history traitsar ereviewed .Th eecologica l implication is explained of thelytoky (automictic or apomictic), arrhenotoky, amphi- toky, sexual reproduction, and semelparity, iteroparity, seasonal itero- parity and therelationshi p between semelparity andjuvenil e development. Several forms ofsynchronizatio n of life-cycleswit h environmentalcondi ­ tions are classified, ranging from the ability to overcome harsh periods duringth eseaso nt oobligat e diapausedormancy .Ecologically ,thi sinvol ­ vesadaptation st oenvironmenta lcondition srangin gfro mirregularl yoccur ­ ring and unpredictable to regularly occurring and predictable. Dispersal traitsar egroupe di ndirectiona lmigratio n (phoresy)an dundirectiona lmi ­ gration (anemochory).A distinction ismad ebetwee n facultative and obli­ gatephores y andbetwee n carrier-specifican dcarrier-unspecifi cphoresy . Amulti-dimensiona l system of tactics ispresented ,base d onwell-define d underivedtraits .Thi ssyste mi scompare dt oone -an dtwo-dimensiona lsche ­ mes ofMacArthu r & Wilson (1967), Grime (1977), and Southwood (1977) and toth emulti-dimensiona lsyste mo fStearn s (1976). Forever y tactic,rela ­ tionshipswit h themai nbiotope swher e itoccur samon gspecies ,ar egiven . Examples of species showing certain tactics are givenpe r taxonomie order of microarthropods. The generality of the traits for various groups of organisms and of the classification of life-history tactics developed is discussed.

INTRODUCTION

Many papers have been published on life-history strategies of species duringth epas tfe wdecades .Classification so flife-histor ystrategie sar e useful in analysing the effect ofnatur e management and of the pollution ofbiotope s (Grime et al. 1988), because speciesan d speciesgroup s canb e compared.However ,ther ear estil lver yfe wpaper so nth elife-histor ystra ­ tegies within a group of species sharing commontraits .

15 Microarthropod communities

Thetheor yo fr -an dK-selectio no fMacArthu ran dWilso n (1967)i smain ­ lybase do ndifference samon gspecie si nreproductiv etraits ,i nparticula r thenumbe ro fegg slai dan dth ejuvenil e survival inrelatio nt oth estabi ­ lity of theenvironment . Inth eclassificatio no f lifehistories , species wereplace dalon ga gradien trunnin gfro mr-selecte dt oK-selecte dspecies . However, many species may be found in the middle of the gradient. Grime (1977,1979 )foun dtha tplant shav ecertai n 'K-selected'trait sunde rhars h environments,differen tfro mth eenvironment s typicalo fK-selectio n sensu MacArthuran dWilso n (1967).Consequently ,Grim eadde dstres sselectio n(o r adversity selection as itwa sname d laterb y Greenslade (1983)), defining theplant swit hK-selecte d traits ina hars hnon- Kenvironmen ta sS-selec - ted.Thi sresulte d ina triangl eo fR- ,C- ,an dS-selection ,wher eR-selec - tioncorrespond swit hMacArthu r& Wilson' sr-selectio nan dC-selectio nwit h their K-selection. Southwood (1977) drew attention to the role of the habitat as the templet for ecological strategies. In Stearns' (1976) classification of life-history tactics the templetbecome s multidimensional. Inthi spape r aclassificatio no flife-histor y tactics isdevelope d for mites,whil eCollembol aar euse dt oevaluat eth esuitabilit yo fth eclassi ­ fication for a taxonomically unrelated group. The main components of the lifehistor yo fmicroarthropod sare :1 .reproductio n (sexualreproduction , thelytokous parthenogenetic reproduction, arrhenotokous parthenogenetic reproduction, semelparityan d iteroparity), 2.developmen t (developmental stagesan dfactor stha tcontro ldevelopment) ,3 .synchronizatio n(diapause , aestivation,an dquiescence) ,an dA .dispersa l (mobility,phores yan dane - mochory). Patterns inthes e traitsar edescribe d asa se ttha t constitutes a tactic sensu Stearns (1976) "a set of coadapted traits designed, by naturalselection ,t osolv eparticula recologica lproblems .A comple xadap ­ tation." Special attention ispai d toth e relationships betweenlife-his ­ tory traits and it is discussed whether these are also relevant to other organisms.Th eclassificatio no flife-histor y tacticsdefine dher ewil lb e compared to those of MacArthur & Wilson (1967), Grime (1977, 1979), Southwood (1977, 1988)an d Stearns (1976).

REPRODUCTION

Wayso freproductio nwil lb eemphasize da slife-histor ytraits ,rathe rtha n the number of eggs produced or the initial rate of population increase whichpla y acentra l role inth e theory of r- andK - selection (MacArthur & Wilson 1967). Although eggproductio n isa n important trait,th evaria ­ tionamon gmicroarthropod s inothe rreproductio ntrait si squit ehigh ,and ,

16 Life-history tactics thereby, suitable for classifying tactics.

Sexual and asexual reproduction

Reproduction inmicroarthropod s iseithe r sexual orparthenogenetic .Par ­ thenogenesisca nhav esevera lecologicall yan dgeneticall ydifferen tforms : 1)arrhenotoky :unfertilize degg shatc hint omale s (haploid)an dfertilize d eggsbecom e females; 2)thelytoky : asexual reproduction of females giving female offspring, resulting in clones; 3) amphitoky: a rather peculiar trait combining both thelytoky and arrhenotoky inon e species. Theadvantag eo fsexua lreproductio nove rasexua lreproductio ni si nth e exchange ofallele swhic hresult s incombination s ofgeneti cmateria l that mayb emor efavourabl e forsurvival .I na variabl ebiotope ,geneti cvaria ­ tionprovide sa chanc e thata tleas tsom eo fth eoffsprin gar ewel ladapte d toth eenvironmenta l circumstances ata particula r time.Diploid yo fsexu ­ allyreproducin g animalsca nals omas krecessiv emutation s (orchromosoma l alterations), resulting ina greate r geneticvariability , whichma yb e of possible futurebenefit . Inarrhenotok y sucha maskin g isimpossibl ebecaus e inth ehaploi dmal e anymutatio nunfavourabl e ata particula r timefind sexpressio nan dconse ­ quentlydisappear s (Helle 1965). So,arrhenotok y results infas tselectio n and fixation of favourable alleles.Anothe r advantage of arrhenotoky may bei ncolonization :on eunfertilize d female ina ne wplac eca nproduc emal e offspring, which might, depending on the adult female's survival and the male development rate,mat e and produce female offspring. Arrhenotoky occurs among theMesostigmat a in,fo rexample , Macrocheles muscadomesticae (Pereira& d eCastr o1947 ), amon gth eTarsonemid ai nTarso - cheylidae,Heterocheylidae ,Dolichocybidae, Trochometridiidae ,Pyemotidae , Acarophenacidae,som ePygmephoridae ,som eMicrodispidae ,fe wScutacaridae , most Tarsonemidae and Podapolipidae (Lindquist 1986), in Actinedida in Tetranychinae, Eryophioidea, (Jeppsone t al. 1975), Cheyletus trouessarti (Hughes1976 )an damon gth eAcaridid a in Histiostoma feronarium (Scheucher 1959). In Collembola and Oribatida arrhenotoky does not occur. Apomicticthelytoky ,i.e .thelytok ywithou tchromosom ereduction ,fusio n ofnuclei ,o ran y similarphenomenon ,ma yhav ea numerica ladvantag e above sexual reproduction or arrhenotoky because a female gives rise to only females, instead of also producing unproductive males (Williams 1975, Greenwood& Adam s 1987). Ina constan tbiotop e itha sth eadditiona ladvan ­ tageo fminima l genetic loss,wit hdaughter s inheriting theapparentl yfa ­ vourable genome of their mother, and deviations from it (mutations) are rare. However, in a temporally variable biotope, thisma y be adisadvan ­ tage,lik esexua lreproductio n ina constan tbiotope ,becaus eo fth echanc e ofchange s ofth eadapte d genome.I nth eothe r type,automicti c thelytoky,

17 Microarthropodcommunitie s reductiono fchromosom enumber stake splac ean dth ehaploi dnucle ima yfus e into diploid nuclei (OliverJ r et al. 1973), resulting insom egeneti c variation among the progeny, though usually less than in sexual re­ production (Wrensche t al. 1994). Datao nth eoccurrenc eo feac ho fth e types of thelytoky, are sparse.Taberl y (1987b)give s evidence for the occurrenceo fthelytok yo fth eautomicti ctyp ei nPlatynothrus pelcifer and Trhypochthonius tectorum andmayb ethi styp eo fthelytok yi scommo namon g these primitive oribatid mites. Recently, Palmer and Norton (1990) publishedexperimenta lproo fo fthelytok yi nfiftee nspecie so fprimitiv e Oribatida (Desmonomata),bu tdi dno tmentio nth etype .Ther ear en odat a onth etyp eo fthelytok y inth eMesostigmat a (Walter& Olive r 1989). Thelytoky occurs, for example, among the Oribatida in Platynothrus peltifer, Trhypochthonius tectorum (Taberly 1987a), Tectocepheus velatus (Grandjean 1941), Oppiella nova (Woodring & Cook 1962, sub Oppia neerlandica) and Microppia minus (Luxton 1981); among theCollembol ai n Isotoma notabilis, Isotomiella minor and some Tullbergiinae (Petersen 1980); among the Mesostigmata in Uropoda minima (Athias-Binche 1981), Rhodacarus denticulatus and Protogamasellus mica (Walter& Kapla n 1990); amongth eActinedid a in Bryobia praetiosa, Brevipalpus obovatus (Jeppson et al. 1975), Tetranycopis horridus (Helle& Bollan d1967 )an d Cheyletus eruditus (Hughes 1976); and among the Tarsonemida in the amphitokous speciesliste dbelow ,an di n Tarsonemus virgineus (Lindquist 1986). Amphitokyseem sa suitabl etrai tfo rth ecolonizatio no frathe rconstan t biotopes:arrhenotok yfo ra fas tselectio no fth egenom eadapte dt oth ene w environmentan dthelytok yt oquickl ypopulat ethi senvironment .I na com ­ parable way the sexual reproduction of the overwintering generationo f speciestha treproduc eb ythelytok y inth esumme rca nb eunderstood .Th e best adapted genome of the next summer season is thereby selected and throughout the favourable season the species exploits thebiotop emos t efficiently by reproducing thelytokously,a s inholocycli c aphids (Heie 1980)an d cladocerans (Ruvinsky et al. 1978). InRotifera , thelytokous generationsdurin gsumme rar ealternate db ya narrhenotokou sgeneratio ni n autumn(Alla n1976 ).I ti sno tknow nwhethe ra seasona lpatter nals ooccur s inmites .Dat ao nthi salternatio no freproductio ntrait sar elacking ,bu t the phenomenon may be expected in some tarsonemid or eryophiidmites , because inthes etax abot hthelytok yan darrhenotok yoccur . Amphitokyhas , forexample ,bee nobserve di n Tarsonemus (= Phytonemus) pallidus by Karl (1965a), in Tarsonemus (= Iponemus) confusus by Karl (1965b)an di n Tarsonemus fusarii bySchaarschmid t (1959); th efirs tegg s laidb y the female were reported to give rise to males, later onest o females. Thesuitabilit yo fth evariou sreproductio ntrait si nspac ean dtim ei s summarized inFigur e2.1 .

18 Life-history tactics

Persistence of population

maintenance establishment

sexual reproduction

Figure 2.1. Types of reproduction placed in a quadrant containing the persistence of population and biotope.

Semelparity and iteroparity

Inadditio nt oth ekin do freproduction ,th ewa yo fovipositio ni sa nimpor ­ tantlife-histor y trait.Here ,iteroparity ,spreadin govipositio n intime , is compared to semelparity, oviposition on one occasion. Iteroparity inmicroarthropod s may be assumed tob e the basic form of oviposition. The reasons for this assumption are: that it does not imply thenee d for (1)morphologica ladaptatio n (sucha sphysogastry , i.e. swel­ ling of the abdomen), (2) a high energy expenditure that comes with the production of offspring in a short period, which could affect survival (sucha si nsemelparity )an d (3)extr aoverwinterin g oroversummerin gwit h the risk of not reaching the next favourable season (such as in seasonal iteroparity). Derivation of this basic type either in the direction of semelparity or of seasonal iteroparity (Bell 1976) would require extra investments, which will only pay off when they lead to an increase in individual survival. Semelparity inmicroarthropod slimit sth eovipositio nperio dt oth emos t favourable part of the season or of the life cycle of the host, as in Iponemus species parasitizing eggs of the bark beetle Ips (Lindquist & Bedard 1961). Another advantage may be the resulting aggregation ofoff ­ springwhic hmigh thel pdecreas ewate r loss invulnerabl e individualsjus t afterhatchin go rmoultin g (Joosse& Verhoe f 1974).A disadvantag e istha t the risko feg gprédatio nma yb ehighe r thanwit h iteroparity.A disadvan ­ tageo fiteroparit y isth euncertaint ywhethe rth etota lreproductiv ecapa -

19 Microarthropodcommunitie s citywil lb eused .Charno van dSchaffe r (1973)poin tou ttha titeroparit y isassociate dwit ha relativel y longadul t lifetimewit h lowmortality . Reductiono fth eag ewhe nth efirs treproductio ntake splace ,whic hbene ­ fits semelparity (Cole 1954), will be dealt with in the section on development. Derivations of thebasi c (iteroparous)for mar eno tver y common.Th e vastmajorit yo fmicroarthropod shav ea novipositio npatter nbetwee nsemel ­ parity and seasonal iteroparity. Semelparity is found for instance in physogastricTarsonemid asuc ha s Siteroptes graminis (Krczal1959) .Adul t femalephysogastr yoccur si nPyemotidae ,Dolichocybidae ,Trochometridiidae , Acarophenacidae,som ePygmephorida ean dPodapolipida ean da fe wmember so f Microdispidae, Scutacaridae, and Tarsonemidae, for instance the genus Iponemus (Lindquist1986) .Tendencie st osemelparity ,expresse da sincrea ­ singnumber so fegg spe rbatch ,occu rt osom eexten ti nCollembola .Synchro ­ nizationo freproductio no fa whol epopulatio noccur sdefinitel y inCol ­ lembola:i n Orchesella cincta, moultingi ssynchronize dafte ra perio do f starvationan drenewe dfoo davailabilit y andwit hmoulting ,reproductio n issynchronize d (Joosse1969 ,Jooss e& Veltkam p1970) . Atth eothe ren do fth egradient , Neoribates gracilis mayb efound ;thi s oribatidmit eha sa ver ylon gadul tlifetim e (Travé& Dura n1971 )an dma y reproducei nsevera lyears .Apar tfro m Neoribates gracilis, seasonalitero ­ parityonl yoccur si na smal lnumbe ro foribati dmites .

DEVELOPMENT

Developmenttim eca ntak ea slittl ea sthre eday su pt oeve nthre eyear s anddepend spartl yo nenvironmenta lfactor ssuc ha stemperatur ean dqualit y offood ,bu twit ha stron ggenetica lbasi seve ni ngeographica lform so f aspecies .Also ,a relationshi pbetwee nag eo fmaturatio nan dclutc hsiz e hasbee ndescribe d (Cole1954) .Variation s indevelopmenta l timeinduce d byth eenvironmen tar esmalle r thanvariatio n inth edevelopmen ttim eo f microarthropodswithi nfamilie so rorders .

Thegeneti c templet ofth ehighe rtax a

Inmite sth etypica ldevelopmen tstage s(o rstases )ar eegg ,larva ,proto - nymph, deutonymph, tritonymph, and adult. This is found inOribatida , Acarididaan dman yActinedida .Mesostigmat alac kth etritonymp hstase ,i n Actinedidaofte nonl ytw ofre enympha lstase sar efoun d(Rhaphignatoidea , Tetranychoidea,Cheyletoidea )an dsometime seve nonl yon enymp h isfoun d

20 Life-historytactic s

(Eriophydoideaan dTrombidoidea) .Tarsonemid alac kal lnympha lstase san d thusonl y gothroug h thelarva lstase .Furthe rreductio n infree-livin g juvenilestase si sfoun di nparasiti cmites ,suc ha sPodapolipodida ewher e adultshatc hdirectl yfro mth eegg ,an di na numbe ro fspecie so fth eAca - rophenacidae, Pyemotidae and Dolichocybidae where adults are born from adultfemale s (Vande rHamme n1972 ,Lindquis t 1986).Juvenil estase sma y notb edroppe dentirely ,a si nman y speciesth e"missing "juvenil estas e isa calyptostase ,developin gan dmoultin gwithi nth epreviou sstase .Th e pre-larvai nActinotrichid ai salway sa calyptostase ,a sar eth eproto -an d tritonymphi nHydrachnella ean dTrombidoidea .A nintermediat eform ,free - livingbu tno tver ymobil eo nit sown ,i scalle dth eelattostase ,suc ha s someo fth ehypop i (deutonymphs)i nAcaridida .I ti sno tlikel ytha tth e occurrence of calyptostases or elattostases speeds up development.Th e function of the kind of development isprobabl y synchronization (inert hypopus of Acarus Immobllis) or dispersal (activehypop i inman y other Acaridida),whic hwil lb edeal twit hi nth enex tsections .

Foodqualit yan dtemperatur e

Themagnitud eo fvariation si ndevelopmen ttim ewithi na specie scause db y differences in the quality of food is limited. Stefaniak and Seniczak (1981)foun da 1. 4time sfaste rdevelopmen ti n Oppia nitens onth efungu s Pénicillium spinulosum thano n Cladosporium herbarium. Waltere t al. (1987) found in Gamasellodes vermivorax and Cosmolaelaps vacua arespectivel y 1.4 and 1.2 times faster developmentwit hnematode s thanwit h arthropodsa s food.Temperatur eha sa mor eobviou seffec to nth erat eo fdevelopment .I n Hypogastrura denticulata, Hale(1965b )foun da 2. 1time sfaste rdevelopmen t during the first five moults at 15°C than at 8°C. In Mesostigmata, Hypoaspis aculeifer takes30-33 ,13-20 ,11-1 9an d5 day sfo rdevelopmen t at13° ,18-20° ,24 °an d28°C ,respectivel y(Kar g1971) .Fashin g(1979 )list s development times at various temperatures of three acaridid mites: Tyrophagus putrescentiae, Caloglyphus anomalus and Naiadacarus arboricola atvariou stemperatures .A nincreas ei ntemperatur efro m20 °t o25° Cwil l speed up development in T. putrescentiae 1.3 times,i n C. anomalus 1.2 times, and in N. arboricola 1.8 times. For Oribatida examples of temperature-dependentdevelopmen tar egive nb yNannell i (1975)fo r Oppia concolor, Bhattacharya et al. (1978) for Oppia nodosa (-Lancelalmoppia nodosa) andTrav éan dDura n(1971 )fo r Neoribates gracilis. InTarsonemid a datafo r Steneotarsonemus spinki axe presentedb yChe n et al. (1979)an d inActinedid a for Tetranychus mcdanieli by Tanigoshi and Logan (1979). Thus,bot htemperatur ean dfoo dqualit yinfluenc eth erat eo fdevelopmen t ina species ,bu tthes edifference sar esmalle r thandifference sbetwee n speciesfro mth esam etaxonomica lorder .I nOribatid adevelopmen ta t18° C

21 Microarthropod communities

ranges from3 3day si n Oppia concolor (Nanneli1975 )t o40 0day si n Stegan- acarus magnus (Webb 1977). Fashing (1979)give sa nexampl eo fa comparati ­ vely slow developing acaridid species Naiadacarus arboricola takes17. 2 daysfo rdevelopmen twhil e Caloglyphus berlesei, C. anomalus and Tyrophagus putrescentiae need5.4 ,5. 7an d7. 3day sa t25°C ,respectively . Naiadacarus arboricola hasi ncommo nwit h S. magnus thecomparativel y lowqualit yo f food ituse s init sbiotope . Most species areunabl e tochang e toothe r foodsource s (Chapter 4). So,foo dqualit y mightbot hhav ea direc t effect on development timean dac ta sa selectiv e force;th epric e ofusin gth e low quality food isa slowe r development. Thus microarthropods ingesting foodwhic hi shar dt oobtain ,o ronl yavailabl ei nsmal lamounts ,o rdiffi ­ cultt odiges tma ynee da comparativel y longertim efo rdevelopment .O nth e otherhand , fastdevelopmen t isonl ypossibl ewhe nfoo di sabundan tan do f highquality .A nexampl ei s Macrocheles muscadomesticae, whichneed sthre e dayst odevelo p fromeg gt oadul t (Wade& Rodrigue z 1961). Thi sspecie si s synchronized withit scarrie r (seesectio no ndispersal ). Sufficien t data lackt opresen t reactionnorm s (Stearns 1992:th erespons eo fth eorganis m toenvironmenta lvariation ),bu tfro mth evariet ypresen tdat aclearl ysho w it isno tunlikel y that reaction norms mayb e crossing. It means that speciesA ma ydevelo p inenvironmen t afaste r than speciesB ,

eo •Sminthurus viridis eggs

30. Hypogastrura denticulate

-Hypogastrura viatica •Folsomia Candida • 1 sotoma viridis

•Onychiurus furcifer Onychiurus latus

-Onychiurus tricampatus Folsomia similis •Onychiurus procamp •Sinella curviseta •Tomoceru s minor Orchesella cincta • 25 30 35 40 45 50 55 60 65 70 days Juvenile development

Figure 2.2. Age at first reproduction plotted against batch size in Collembola at 15°C. Data are from Davidson (1934), Hale (1965a), Hutson (1978), Joosse and Veltkamp (1970), Hertens et al. (1983), Niijima (1973), Sharma and Kevan (1963), Snider (1983) and Witteveen and Joosse (1987).

22 Life-history tactics but inenvironmen tb slower thanspecie s B.Thi spreclude s theus eo fthi s trait ina classification.

Relation to semelparity

Minimizingag ea tfirs treproductio nbenefit ssemelparit y andlarg eclutc h size (Cole 1954). So, are species with a short development period less iteroparous thanothers ? Ingamasi dmites ,female susuall y carry only one egg (Karg 1971), but the fast developing Arctoseius cetratus (12.5 days from egg to adult at 22°C:Binn s 1974)yield s ahighes t daily total of 13 eggs per female (mean 2.5 eggs.female"1.day" 1 (Binns 1974)). On the other hand, Pergamasus robustus takeso naverag e43. 5day s fromeg gt oadul tan d the oviposition period isquit e long,yieldin g an egg production of 0.25 egg.female"1,day" 1(Bhattacharyy a 1963).Fo rCollembola ,ag ea tfirs trepro ­ ductiona t15° C inlaborator y experiments isplotte d inFigur e 2.2 against thenumbe r ofegg s perbatc h at the same temperature. The relationship is significant (linear regression:p<0.05 )fo rspecie sfo rwhic hvalue scoul d be obtained. Note the difference inth e definition ofbatc h as thenumbe r of eggs deposited at the same time at the same place, and that of clutch inVa nStraale nan dJooss e (1985)an dJansse nan dJooss e (1987)a sth enum ­ ber ofegg s laiddurin g areproductiv e instarperiod . These clutchvalue s areusuall ybigger ,an dma yconsis to fsevera lbatches ,wit ha considerabl e variation inhatchin g time. Hence, in Collembola a relationship exists between minimizing age at first reproduction and a less iteroparous reproduction.

SYNCHRONIZATION

Thelif ecycl eo fa specie sca nb esynchronize dwit hth eenvironmenta lfac ­ tors most important for that species. These environmental factors can be abiotic, synchronizing the life cyclewit h thecycli c period in the envi­ ronment, or the "environmental" factors may be biotic; synchronizing the species'lif ecycl ewit htha to fit scarrie r (inphoretics )o rhos t (inpa ­ rasites)thu sbein gno tnecessaril y seasonal.I wil lfocu sher eo nseasona l synchronization and dealwit h synchronization to carriers in the section ondispersal .Restin gstage sca nb equit eprimitive ,know na snon-diapaus e dormancy, or have a solid physiological basis,calle d diapause dormancy.

Non-diapause resting stages

Specieshav edevelope dal lkind so fsolution s forovercomin g unpredictable

23 Microarthropodcommunitie s

orpredictabl eunfavourabl eperiod si nth eenvironment ,suc ha smovin go n andsettlin gelsewher eo rwithstandin ghars hconditions .Microarthropod s hardlymigrate .Th elocomotor ycapacit yo fmos tspecie s islow .Vertica l movement,however ,doe soccu ran di sa wa yo fescapin gfro mdesiccation , orfro mver ylo wo rhig htemperature s (Metz1971 ). SomeCollembola ,Oribatida ,an dActinedid ahav edevelope d theabilit y ofsupercooling ,a physiologica lproces so faccumulatio no fpolyol s(glyce ­ rol)i nth ehaemolymph ,whic hgive sth eanima la bette rchanc eo fsurvivin g temperatures below the freezing point of their haemolymph (e.g.Somme , 1981).Thes especie sar eprimaril y(ant)arcti co ralpine ,bu tals oth etem ­ perateOribatid a Carabodes labyrLnthicus, Fuscozetes fuscipes and Ceratop- pia bipilis areamon gthos e listedb y Somme (1981). A longperio dunde r harshcondition swithou tfoo dwil levolv et oquiescence ,whic hi sdefine d byTaube re t al. (1986)a s" areversibl estat eo fsuppresse dmetabolis mim ­ posedb ycondition sbeyon dcertai nthreshold si ntemperature ,moistur ean d nutrition".Wheneve rquiescenc eha sa seasona lbasi si ti scalle dnon-dia ­ pausedormanc y(Taube re t al. 1986),occurrin gfo rinstanc ei nth eoribati d Alaskozetes antarcticus (Young& Bloc k1980) .Mesostigmati dmite sgenerall y havecontinuou sgenerations ,bu ti nth eterrestria lmesostigmati d Zerconop- sis miistairi theegg sca novercom ea lon gperio do ffresh-wate rsubmergenc e (upt o12 8days) .Th esam ehold sfo rth eactinedi d Cheylostigmaeus panno- nicus andsom eCollembol a (Tamm 1984).Acaridi dmite sovercom ehars hpe ­ riodsa shypop i(deutonymphs) ,fo rexampl e Acarus immobilis (Hughes1976) .

Diapausedormanc y

Realdiapaus et oovercom ea hars hseaso ni srathe runcommo ni nsoi lmicro - arthropods.Wher ei toccurs ,diapaus edormanc yha sevolve di nusuall yon e buti nsom ecase smor elif estages .I nCollembol asom especie soverwinte r asdiapaus eegg s(Blancquaer te t al. 1981),bu tmost ,especiall yeuedaphic , specieshav econtinuou sgeneration san dn odiapaus ea tall ,comparabl et o mostoribati dmites .I nTarsonemida ,adul tfemale soverwinte r (Lindquist 1986),bu ti ti sno tclea rwhethe rthi si sa rea ldiapause .Th ever yhete ­ rogeneousactinedi dmite shav evariou sway so fovercomin ga hars hseason . Insom especie so fEryophyoidea ,th enorma lfemale salternat ewit hdeuto - gynesi na hars hseason .Thes edeutogyne soccu ri nspecie sfro mtemperat e andarcti c latitudesan dhav e tob e subjected towinte r chillingbefor e theyca nreproduce :a rea ldiapaus edormanc y (Jeppsone t al. 1975).Als o theTetranychida ean dmite so fsom eothe rfamilies ,pas sth eunfavourabl e seasona sadul tfemales ,bu tsom etetranychid san dsom especie sfro mothe r familiesoverwinte ra sdiapaus eegg s (Jeppsone t al. 1975). Summer diapause oraestivatio noccur s inth eeg g stage inEupodoide a (Halotydeus destructor) (Wallace 1970) and inTetranychoide a (Petrobia

24 Life-historytactic s latens) (Jeppson et al. 1975)amon g theActlnedida . InCollembol aNaj t (1983)an dJooss e(1983 )reporte decomorphosi si nHypogastrurida ean dIso - tomidae:adult ssho wmorphologica lan dphysiologica lchanges ,cree pawa y in deeper soil layers and starve. Barra and Poinsot-Balaguer (1977) described another adult adaptation to summer drought in Collembola: anhydrobiosis.I ncontras twit hecomorphosis ,anhydrobioti canimal sbecom e activea ssoo na ssoi lmoistur econdition sar efavourabl eagain .However , mostspecie sovercom eth edr yseaso ni nth eeg gstage .

DISPERSAL

Inmicroarthropod s dispersalb yactiv e locomotioni so fmino rimportanc e comparedwit hdispersa lb ywin d (anemochory),b ywater ,o rb yanima lcar ­ riers,mostl y insects (phoresy).Zachvatki n (1959)measure d 5.2mm.min" 1 for Caloglyphus rodionovi (= C. berlesei (Michael1903) )u pt o15 0mm.min" 1 for Glycyphagus (=Lepidoglyphus) michaeli (Oudemans1903 ).Man ypredator s (Gamasinaan dActinedida )mov efaste rbu tthei rmovement sar eseldo mi na straightline ,thu scoverin gshor tdistance sonly . Phoresyo ranemochor y arelife-histor y traitst ob econsidere d inth e classificationo flife-histor ytactics .Unlik ephoresy ,anemochor ywil lb e associatedwit hhig heg gproduction .Mitchel l (1970)rank s Tetranychus - Poecilochirus - Iponemus (resp.anemochoric ,phoreti ccarrier-unspecific , andphoreti ccarrier-specific )accordin gt oth eprobabilit yo fdiscoverin g ane wresource .Phores yha sno tye tbee nrecorde di nCollembola ,thu sth e nextsectio nonl ydeal swit hmites .

Phoresy

Farishan dAxtel l (1971)defin ephores ya sth e "phenomenon inwhic hon e animalactivel yseek sou tan dattache st oth eoute rsurfac eo fanothe rani ­ malfo ra limite dtim edurin gwhic hth ephoreti c ceasesbot hfeedin gan d ontogenesis,suc hattachmen tpresumabl yresultin gi ndispersa lfro marea s unsuitedfo rfurthe rdevelopment ,eithe ro fth eindividua lo rit sprogeny" . Insom eoccasion sth ephoreti cma yhav ebee nobserve dfeedin go nth ecar ­ rier(Jali l& Rodrigue z1970) .I ti squestionabl ewhethe rphores yi salway s initiatedb ya nexpecte ddegradatio no fth ebiotope ,a sman yphoretic sliv e inbiotope s thatexis t longer thanon e generationperio d (forinstance , nidicolousan dcorticolou sspecies) . Dispersali nmite sma yoccu ri nver yspecifi cways .Whe na mit eattache s toa hos t (mostlya ninsect) ,tha tcarrie si tt oanothe rplace ,th emit e

25 Microarthropodcommunitie s iscalle dth ephoreti can dth ehos ti scalle dth ecarrier .Binn s(1982 )re ­ viewsphores yextensively .Here ,I conside ronl ya fe wo fit secologica l aspects: the lifestag eo fth ephoretic ,whethe r orno tsynchronisatio n withit scarrie rtake splace ,whethe ro rno tth ephoreti ci scarrie rspeci ­ fic, andwhethe rphores y isobligate ,facultativ eo rjus taccidental .I n manypaper s(cf .Binn s1982) ,accidenta lphores yrefer st oth erelationshi p betweenth ephoreti can dth ecarrier .However ,I us eaccidenta lphores yt o expressth ephoreti cmovemen to fa specie stha ti sseldoml yphoretic .

Life stage of the phoretic

Without exception, inUropodin a thephoreti c is thedeutonymp h(Athias - Binche1984 )whic hha sdevelope da flexibl estal ka tth erea ren do fth e hysterosoma. Not all uropodids are phoretic (Athias-Binche 1981), for example,som esoi linhabitant so fth egener a Trachytes, Polyaspinus (all species)an d Dinychus (some species). Fora detaile d descriptiono fth e uropodiddeutonymph sse eKar g (1989). Also inth eAcaridid a thephoreti c isth edeutonymph ,calle dth ehypopus ,whic hi sals ospeciall yadapte dt o cling on a carrier as described in detail for many species by Hughes (1976).Agai nno tal lhypop iamon gth eAcaridid aar ephoretic ;som ehypop i are inert resting stages. They are highly resistant to desiccation (Griffiths1964 )an dothe rform so fstress . Carpoglyphus lactis (Linnaeus 1758) can even pass through the alimentary canal of mice and sparrows (Chmielewski 1970). Thebest-fitte d organism tofoun da ne wcolon y isa non-gravidfertil efemal e(Southwoo d1962 ,Binn s1982) .Adul tphoretic sar e usually females (Jalil& Rodrigue z 1970).Especiall y inth eTarsonemida , phoresyoccur si nthi slife-stag e(Lindquis t1986) .Finally ,i nth eGamasi - na,phores yma yoccu ri neithe rth eadul tlif estage ,fo rexample , Hacro- cheles spp.(Jali l& Rodrigue z1970 ,Krant z& Whitake r1988 )an d Arctoseius cetratus (Binns1974) ,o ri nth edeutonymp ha si n Digamasellus (=Dendro- laelaps) fallax (Leitner1949 )(Binn s1973 )an d Parasitus spp.(Kar g1971) . Furtherinformatio no nassociation sbetwee nMesostigmat aan dothe rarthro ­ podsincludin gparasitis mca nb efoun di nHunte ran dRosari o (1988).I nth e Oribatidaan dActinedid ai nwhic hphores yoccasionall yoccurs ,th ephore ­ ticsar egenerall yadult s (Desender& Vaneechoutt e 1984,Norto n 1980).

Synchronization of phoretic and carrier

Lindquist (1975)distinguishe sfou rtype so fsynchronizatio nbetwee npho ­ retican dcarrier ,al lo fthe madaptation so fth emites .I nth efirs ttype , thelif ecycl eo fth emit ei srestraine ddurin ga nearl yperio do fth elif e cycleo fth ecarrier ;durin gth eeg gan dlarva ldevelopmen to fth ecarrier , theadul tfemal emit eundergoe sa ninactiv epost-phoreti cperiod .Durin g

26 Life-historytactic s theprepupa lstag eo fth ecarrier ,thes efemal emite sbecom eactive ,see m to feed oncuticula r exudates, lay eggswhic h develop during thepupa l stageo fth ecarrie rt oyoun gfemales ,whic hleav eth enes twit hth ene w generationo fcarriers .Skaif e (1952)describe s anexampl eo fthi swit h Dinogamasus braunsi onth ecarpente rbe e Mesotrichia caffra. Ofcourse ,i n thisrelationshi pphores y isobligat ean dspecific . The second type of synchronization is characterized by a restraint duringa lat eperio di nth elif ecycl eo fth ecarrier .Th efemal ephoreti c startslayin gegg sa tth esam etim ea sit scarrie ran dfeed so nit scar ­ rier'seggs .Th eegg san dlarva equickl ydevelo pint oa ne wgeneratio no f youngmites ,whic hwai t3- 6week swithou tfeeding .Thi styp eo fsynchroni ­ zationi sdocumente db yLindquis t (1969)fo rsevera lspecie so f Iponemus, whichar eal lver ycarrie rspecifi can dobligat ephoretic so nipin ebark - beetles. Thethir dtyp eo fsynchronizatio ni sth einterruptio no fth emite' slif e cycledurin ga perio dbetwee nth egeneration so fa carrier .Th ephoreti c herei sth ejuvenil estag e (deutonympho rhypopus )waitin gfo ra carrier . Therelationshi p isno tnecessaril ycarrie rspecific ,an ddeutonymph sca n attach to any organism entering thebiotop e (Binns 1972) and also the deutonymph stage canb e omitted, thus resulting in facultative phoresy (Binns1982 ). Thefourt htyp eo fsynchronizatio ni sa rac eagains ttime . Macrocheles muscadomesticae develops in three days from egg to adult and itsmai n carrier Musca domestica takestw oday st oreac hth esecon dinstar ,whic h isimmun et oprédatio nb yth emites ,tha tfee do nth eegg san dfirs tinsta r larvaeo fth efl y (Wade& Rodrigue z 1961).

Obligate and facultative phoresy and carrier-specificity

Inphoresy ,a tren dca nb eobserve dfro moccasiona l transport toregula r transport diverging into two pathways.Th e first is carrier unspecific biotope-dependentsuc ha si n Arctoseius cetratus, anadaptatio nendin gwit h the synchronization in development of Macrocheles muscadomesticae with fliessuc ha sth ehousefl y (Wade& Rodrigue z 1961), oneou to fmor etha n adoze no fcarrier s(Hunte r& Rosari o1988) .Th eothe ri scarrie rspecific , rangingfro mspecie ssharin gth esam ebiotop ea sth ecarrier ,suc ha si n Dinogamasus braunsi, whichfeed so nth eegg so fit scarrie ran dremain sa relativelyshor tperio do nth ecarrie r(Skaif e1952) ,t ospecie swhic har e calledparasites ,onl yleavin gth ehos tt oreproduce ,o reve nreproducin g onth ehos titself ,suc ha si n Sarcoptes spp.an d Demodex aurati (Nutting 1964)i nth eAcaridida ,an dSpinturnicida e(Sweatma n1971 )i nth eMesostig - mata.Specie so fth elatte rcategorie sma ysho wsom eparenta lcar ei nth e formo flarviparit y(Dolichocybidae ,Pyemotida ean dfe wPygmephorida eamon g

27 Microarthropod communities theTarsonemida )(Lindquis t1986 )o reve ngiv ebirt ht oadult s (Acarophena- cidae in the Tarsonemida, such as Acarophenax tribolii) (Hughes 1976). Phoresy inth ecas eo f Musca and Hacrocheles isobligate ,a sth ebiotop e does not exist long enough for the development of more mite generations, but probably not carrier specific. The fast development of the mite is favouredb yhig hqualit y ofth efoo d (seeth e sectiono ndevelopment) . The functiono fth efas tdevelopmen to f the flydurin g theeg gstag ean d first larval instar seems to escape from acarine predators occurring in such biotopes.Amon g oribatidmite sphores y isprobabl y accidental;hardl y any species relies onphores y in its lifehistory . Exceptionsma yb e thewoo d inhabitingoribati dmite sliste da sphoretic sb yNorto n (1980), especiall y the Mesoplophora spp.,clingin g to insect hairs.A parallel may be found in Naiadacarus arboricola that lives in waterfilled tree-holes (Fashing 1975)an dothe r inhabitants ofdiscret ebiotope s sucha snest so fmammals , birds, and ants. Phoresy in these cases may be facultative, because the biotoperemain sintac tfo rsevera lgenerations ,an di sno tnecessaril ycar ­ rier specific. InActinedid a mites of the family Cheyletidae are phoretic (VanEyndhove n1964 )suc ha s Cheyletomorpha lepidopterum (Shaw1794) ,whic h isphoreti c inth eadul t stagean dphores y isprobabl y facultative andno t carrier specific.

Persistenceo fpopulatio n

continuous discontinuous

continuous diapause or «u « continuous generations u Q. quiescense c o

•5-° anemochory «>o discontinuous facultative phoresy Q- obligate phoresy

Figure 2.3. Types of synchronization and dispersal in microarthropods placed in a quadrant containing persistence of population and biotope.

Analogous to Southwood's (1977) time-space quadrant, Figure 2.3 shows atime-biotop equadran twit htrait stha tma yhav esurviva lvalu eunde rdis ­ continuityeithe r inbiotope ,o ri ntime .Specie slivin gi ncontinuou sbio -

28 Life-historytactic s

topes,suc ha sfores tsoils ,nee dn ospecia ladaptation si nthei rlif ehis ­ toryi nterm so fdiapaus e (tobridg ea nunfavourabl epar to fth eseason ) ormigratio n (tobridg ea nunfavourabl espac et oth enex tfavourabl ebio - tope).I fth epersistenc eo fth epopulatio ni sdiscontinuous ,i.e .whe nun ­ favourablecondition sdurin gpar to fth eyea rexist ,the nadaptation ssuc h asdiapaus eo rquiescenc ehav esurviva lvalue .Discontinuitie si nth eblo - topeca nb esolve db ymigratio ni nmicroarthropods ,especiall yb yphoresy . Phoresy,combine dwit hcomparativel ystabl ebiotope s(continuou san dover ­ lappingi ntime) ,ca nlea dt ocarrier-specificity ,possibl ywit heg gpara ­ sitism.Tim espen to nth ecarrie ri srelativel yshort ,a si n Vidia concel- laria (McNulty1971 )an di n Dinogamasus braunsi (Skaife1952) ,an dalway s predictable.Biotop eexample sar edecayin gwood ,an dnest so fants ,birds , andmammals . Discontinuity inbot h timean dbiotop e refers toephemera l biotopessuc ha scarrio nan ddung-patches .Phores yher ei slikel yt ob eun - specific,e.g . in Macrocheles muscadomesticae (foundo n1 6dung-visitin g flyspecies ;Hunte ran dRosari o1988 )althoug ha synchron yha sevolve dwit h thedevelopmen to fit smai ncarriers .Tim espen twit hth ecarrie rma yb e either long or short,bu t isunpredictable . For example, Poecilochirus necrophori isphoreti co nbot hth ecarrio nbeetle s Necrophorus humator and N. Investigator; deutonymphssta yi nth epupa lcel lo fth ecarrie rdurin g a pupation of either 2 (N. humator) or 10 months (N. investigator) (Springett 1968). P. necrophori mayb ea nexampl eo fwha tStearn s (1976) calledspecie sadapte dt ononcycli cbiotopes ,i.e .biotope sdistribute da s randomvariable s intime .

Anemochory

Anothermajo rfor mo fdispersal ,anemochory , isfoun di nth eActinedida , especially inth eTetranychoide aan dEriophyoide a (Jeppson et al. 1975). Compared to phoresy, where the phoretic is usually carried to a new exploitablebiotope , inanemochor y the losso f individualswhic hd ono t reacha ne wfavourabl ebiotop ei sreporte dt ob eove r9 0pe rcen t(Jeppso n et al. 1975).Thes eanemochori cspecie swil lgenerall yhav ea highe rrepro ­ ductiverat etha nphoretics ;fo rexample , Tetranychus urticae Kochproduce s 90-110egg spe rfemal e(Jeppso n et al. 1975),an dth ephoreti c Dinogamasus braunsi, 5-10egg spe rfemal e (Skaife1952) .

BOUNDARIESAN DTRANSITION S

Iti sclea r from thepreviou s sections thata life-histor y traitcanno t

29 Microarthropod communities

easilyb ecalle dr-selecte do rK-selected .Th ewa yth etrai ti suse ddeter ­ mines how itfit s into the tactic asa whole ; itca nb e used as an answer to completely different environmental problems. Phoresy for instance is commonly seen asa 'r-selected' trait (Binns 1982;Hunte r &Rosari o 1988) butmos t ofth e carrier-specific facultative phoretics inFigur e 2.3 have arathe rlo weg gproductio nan dofte nothe rtrait stha twoul dclassif y them asK- ,rathe rtha nr-selecte d (Fashing1975 ,1979 ;reportin go n Naiadacarus arboricola) .Likewise , Mesoplophora spp.d ono tsho wr-selecte d traits,bu t nevertheless arephoreti c (Norton 1980). Sophores y seems tob e an answer both forrapi d colonization andexploitatio n ofephemera l biotopes occur­ ringrandoml y intim ean dplace ,an dfo rcolonizatio no fdiscretel ydistri ­ butedbiotopes ,whic hma ypersis tfo rman ygeneration s ofmicroarthropods . The slowdevelopmen t of Naiadacarus arborlcola may inpar tb e anadap ­ tationt oth elimite dfoo dresource sa sindicate dfo rman yOribatid ai nth e section ondevelopment . In thesecircumstance s the slow development trait canhardl y be considered K-selected, as Fashing (1979) does, because the limited foodqualit y isno tdu e tocompetition .Rathe r itshoul db e called S-selected inth e sense ofGrim e (1979), because it isa nadaptatio n to a harsh aspect of the environment. Lowtemperature ,anothe rhars haspec to fth eenvironment ,als olead st o slowdevelopment .Eve nquiescenc e forms, sucha ssom ehypop i inth eAcari - dida or some deutonymphs in the Mesostigmata, may be classified as forms of slow development. Again this is an example where the function of one trait, slowdevelopment ,ca nb e tomee t different environmental problems: a cold period, a dry period, or low food quality. Different answers for the same environmental problems are well known. Solutions to environmental changes are either migration, ordiapaus e ora combination ofboth ,dependin g on the reversibility and regularity of the environmental changes (Southwood 1962). Regula r changes lead to diapause forms and irregular changes tomigration . Another example of a different answer to the same environmental problem mayb e seen inmigratio n itself. A favourable biotope for the continued existence of a population may be reached by random migration accompanied by a high reproductive rate associatedwit h ahig hnumbe r ofcasualties ,o rb y directional migration, as inphoresy ,whic h isonl y accompanied by ahig h reproductive rate when the favourability of the newbiotop e isuncertain . Hence,i twoul d seemtha tsimpl e systems torepresen t life-history tac­ tics such as the one-dimensional continuum of the r- toK-axi s (MacArthur & Wilson 1967)o r the two-dimensional systems ofth eR- , C-an dS-triangl e (Grime 1977, 1979, Grime et al. 1988) and the space-time quadrants (Southwood 1977)ar e too simple. Themultidimensiona l systemo fStearn s (1976)i sno tsuitabl e torepre ­ sentth elife-histor ytactic so fmicroarthropod seither .Multivoltinit yi s

30 Life-history tactics presented as an adaptation to environmental cycles much longer than the lifespan. Examples ofunivoltin e insects are givenwhe n the cyclic period isabou t equal too r shorter than the lifespan. This suggests thatvolti - nity is an important trait. The number of generations per cyclic period (usually ayea r in temperate regions),however , isno t a trait initself , buti sderive dfro mdevelopmen tan dsynchronization .Fo rexample ,a specie s univoltine intemperat e regions,woul donl ysta yunivoltin e insubtropica l andtropica lregion s ifit slif ecycl eha da nobligat ediapause ,an di nbo ­ realregion s ifit sdevelopmen twa s fastenoug h tocomplet e the lifecycl e within ayear . Species subject tofacultativ e diapause (Tetranychidae)o r withoutan ydiapaus e (Oribatida)ma yb eunivoltin e inborea lregions ,some ­ timeseve ntakin gmor e thanon eyea rt ocomplet e theirlif ecycle ,an dmul - tivoltine intemperate , subtropical,o r tropical regions.Thu s thenumbe r ofgeneration s per cyclic period canonl yb euse d asa life-history trait forclassifyin g life-history tacticswhe n iti saccompanie db ya nobligat e diapause and is thus restricted to the use of obligate univoltinity, or bivoltinity when an obligate aestivation forms part of the life cycle. In conclusion, low dimensional schemes of life-history tactics appear tob eto osimpl ean dth eonl ymultidimensiona lschem epresente di nth elite ­ rature (Stearns 1976) is not well defined in all respects and is conse­ quently of limited use to represent life-history tactics of microarthro- pods.Therefore ,a differen tschem eo fmicroarthropo d life-history tactics isdesigne d below.

LIFE-HISTORY TACTICS

Twelve life-history traits of microarthropods are distinguished: sexual reproduction, thelytoky,amphytoky ,arrhenotoky , iteroparity,semelparit y as reproductive traits;th e relative rate ofdevelopmen t as developmental trait; obligate diapause, facultative diapause and quiescence assynchro ­ nization traits;an dphores y andanemochor y asmigratio n traits.Th ebes t way tomak e such aclassificatio n is toanalys e all traits thoroughly and build up the tactics trait by trait (Harvey & Pagel 1991, Stearns 1992). However, in a field where specified data on life-history traits are scattered I followed an iterative method. For every imaginary tactics species exampleswer e tob e found andfinall y any speciesha d tob e placed ina tacti cwothou tdifficulties .Fo rinstance ,ther ear en omicroarthropo d species combining the traits adult obligate phoresy with thelytoky. This method resulted in twelve life-history tactics (Table 2.1).Th e sequence of traits as presented in Figure 2.4 isno t meant tob e hierarchical.

31 Microarthropod communities

(0 C V V V 0) ^ i-t 0 > 0) > O) v d •H iH y -H O «H y C « C 4-> 4J C *J C 4J c 0) 4-> O 4 (4 (d Ü (0 »H > w y 4J U 4-> «J ft rH CO M CA 4-1 •H r-l « rH M r-l fl)0u1 fti- t 3 0) V -i-I «i-I 4J 3

c CD ao *o A y a) C G 4-1 •H > •H et) i-i *4-l 0 u 0 0) •i-l T-I co i-l .H •W U ti « id O) V C vi y y co «00 CO -H -H c •>H •H &^ O 00 60 0 4J i a a. o o -H a) A «M 4-> rH rH V U 0 U (0 -00« rH •H Ù0 W Ä *H P S K U 1-4 •H O J3 T3 m« » a o C S ft n»

O 3 O 4-)

E-t M

32 Life-history tactics

s oP. 4-f m O 4-1

fH 1-1 O *H o3* 3e r^ « 3a*

•H

iJ u u u o a il n 4 W U M H M !x *ao *ov *oa> *ôa> o o o o o -t e e s e

3 3 3 3 3 O O o o o i-H o o « C cd 3 3 3 « 3 3 3 2 c e c c c c O +J O H .,-( „-( Q «H -H U U +J « « W e e c « s c o o oO « «o oO (J

33 Microarthropod communities

-fully zoobiont

-partly zoobiont

phoretic - facultative (mostly carrier specific)

-obligate -as juvenile (mostly carrier unspecific) morphological and physiological adapted

-as adult without special adaptations

not phoretic -synchronization -obligate diapause

-facultative -semelparous diapause or quiescense -iteroparous -anemochorous

-not anemochorous

-no synchronization -thelytokous -slow development

-fast development

-sexual reproduction -continuous iteroparity

-seasonal iteroparity

Figure 2.4. Scheme of microarthropod life-history tactics as they are defined by the main life-history traits.

The limitednumbe ro flife-histor y tacticsrecognize dan dth erelativ ein - sensitiveness to theran k order of traits distinguished implies a high degree ofcorrelatio n between traits.

THE MAIN BIOTOPES PERTACTI CAN DSPECIE S EXAMPLES

The main biotopes ofspecie s with thelife-histor y tactics distinguished above, willb edeal t with briefly. Tactics areassemble d inthre e groups

34 Life-history tactics forconvenience :directiona l dispersal,synchronization , and reproduction tactics, named after their most significant traits. Table 2.2 givesexample s of the tactics atth e species levelwithi nth e main orders of the Acari (Acaridida, Oribatida, Actinedida, Tarsonemida, Mesostigmata)an dth einsec torde rCollembola .Tabl e2. 2show stha tCollem - bolai sth emos thomogeneou sorde rwit hrespec tt olife-histor y tacticsan d that the mite ordersActinedid a andMesostigmat a are themos theterogene ­ ous. Inclusiono fCollembol a doesno t leadt oan yadditiona l tactics.Col ­ lembola generally have a relatively fast development and the only other life-historytrait sdevelope dar ethelytoky , ina larg enumbe ro fspecies , and diapause eggs, ina small number of species. For convenience, inth e review of the tactics,tacti c numbers are pre­ cededb y a short,henc e incomplete, listo f life-history characteristics.

Directional dispersal tactics

Tactic Ii sconfine d toparasite s ofvertebrate s and invertebrates.A dis­ tinction has been made between those living exclusively on the host (la) and those partly free-living for reproduction or dispersal (lb). The spe­ cies showing facultative phoresy (tactic II) are generally species of relatively long existing, discretely distributed biotopes. In this case phoresy serves to colonize new biotopes, but leaving the biotope is not obligatorybecaus e thebiotop ewil lpersis t fora rathe rlon gtime .Carrie r specificity seems thebes tmean s forreachin g thebiotope .A n increase in the development rate is usually not functional, except for achieving synchronization with the carrier, and retarded development may occur because ofsynchronization ,o rhars hconditions ,suc ha slo wfoo dquality . Becauseo fphoresy ,specie swit hobligat ejuvenil ephores y (tacticIII )ar e able to quickly colonize ephemeral biotopes, such as dung pats, carrion, decaying mushrooms, and rotting fruit. Phoresy is obligate due to the transient nature of the biotope, and therefore usually not carrier spe­ cific. The same holds for obligate adult phoretics (tactic IV),bu t the differencebetwee nth etw oi sth eabilit yo fth eadul tphoretic st ocorrec t their arrival in an unsuitable biotope by taking another carrier to the nextbiotope . Parasitic forms occur in all mite orders except Oribatida. Phoresy occurs inal lmit eorder san d iseithe rfacultative ,o rwhe nobligate ,the n carrier specific, with relatively slow development. Obligate juvenile phoresywit hphysiologica l andmorphologica l adaptations isrestricte d to Acaridida and Mesostigmata, while obligate adult phoresy, mostly carrier unspecific, seems tob e restricted to the Mesostigmata.

35 Microarthropod communities

Synchronization tactics

Species with anobligat e diapause (tacticV )ar e either univoltine orbi - voltine (having both an obligate diapause and an obligate aestivation in alternategenerations );the yar ehighl ysynchronize dwit hth eseason ,whic h isusuall yaccompanie db ya hig hreproductiv esuccess .Synchronizatio nwit h thebiotop e isrealize d intw oway s inspecie swit ha combinatio no ffacul ­ tativediapaus e andsemelparit y (tactic VI). Specieswit hfacultativ edia ­ pauseo rquiescens e (tacticVIII )combine dwit hanemochor y (tacticVII )ca n easily overcome unfavourable periods in the environmentalcycle . Obligatediapaus ei srestricte dt oth eActinedid aan dCollembola .Facul ­ tative diapause and semelparity occurs in the Tarsonemida and Collembola only. Facultative diapause or quiescense with anemochory occurs in some Mesostigmata and in the Actinedida (Tetranychidae and Eryophiidae). Syn­ chronization inMesostigmat a refers toquiescenc e and inTetranychida e to facultative diapause. Sole quiescence or facultative diapause occurs in almost allorders .

Reproduction tactics

The presence of thelytokous reproduction distinguishes tactics IX and X fromX Ian dXII .Specie sreproducin gb y thelytoky canb eexpecte d inquit e constant environments, or environments made constant by human activities by imposing aver yhars h anddominan t constant factor.Unde rne w conditi­ ons, species with thelytoky (tactic X) increase faster than those with thelytoky and seasonal iteroparity (tactic IX); in more established conditions, species with thelytoky overcome disturbance more easily than specieswit h thelytoky and seasonal iteroparity,becaus e of their shorter generation time.Ther e are many species with sexual reproduction (tactic XI) that canb e found inalmos t anybiotop e insoi l orvegetation . Sexual reproduction and continuous iteroparity result inspreadin g the risko fa complete loss of offspring. Spreading the risk of harsh events is even better in sexually reproducing species with seasonal iteroparity (tactic XII), where the loss ofa complet e reproductive seasonma yb e permitted. Thelytoky occurs inal l the orders listed, allthough in the Acaridida thelytoky may occur only in combination with facultative phoresy. Sexual reproduction occurs in all orders. Sexual reproduction with seasonal iteroparity seems tob e restricted to the Oribatida.

36 Life-history tactics

VI t semelparit y

VIII t synchronization tactics diapause forms

thelytoky seasonal thelytoky IX* ; — XIM XI ,/v /v -•x " iteroparity I phoresy reproduction tactics

dispersal tactics

special morphological and physiological adaptations of juveniles

Figure 2.5. Scheme of the interrelationships between the life-history tactics defined for microarthropods. For definition see Table 2.1.

37 Mieroarthropod communities

M -1 3 13 •" ï1 u II g -H j) S o « c

-*1 M 3 M I) 6 0» >H a Q m « « -H m •u -H o Q *M s Q< M 3 Q. « "Ö •M *J •1 'fi 0) i) •H -H M •M « a « « 4J OX|*Ö v q (Q nj u 0 Q, D -q •U M .Q fl § •H u u u m v Q, -u VH 01 M •u bi ra D) H 0 11 >1 « 0 Q) tn p « « 0 U 0 M 3 4) M 0 0> n^ •H B M (0 M U U g C C a A c« •9 û. M fi •a m U» -H 0) M Ol Q 0, a P: 1 M S" ty S c •5 e h *

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> H iH tW C •H V .q « u w O £ -•H u 3 J U Q • 3 Û..H U O tM 0 3« -q 1 '1 0 •H 3 B a U V -U û, J i3 o ë » * *

m m m ^ *d 3 •n M a o s q W-lROMOO« V U -H U A 'H -U B •U -M M -ri U I4 VI -r( a,x)4ju«oooî* J3 -H a, B

H M >

38 Life-history tactics

COMPARISON WITH OTHER LIFE-HISTORY TACTICS

Thetwelv e life-history tacticso fraicroarthropods ar eschematicall y shown inFigur e2.5 .Excep tfo rth eclassificatio ngive nb yStearn s (1976),gene ­ ral classifications of life-history tactics are of low dimensionality (MacArthur & Wilson 1967,Grim e 1977, Southwood 1977). The advantage of these theories is their easy accessibility compared to the more complex scheme (Fig.2.5) .T omak eth elife-histor y tacticso fmicroarthropod smor e understandable, they canb eprojecte d onto ther- Kcontinuu m ofMacArthu r & Wilson (1967), th e triangle ofGrim e (1977)an d the time-space quadrant of Southwood (1977), respectively (Fig. 2.6).Th e location of a tactic along ther- K continuumo r inth e triangle dependsver ymuc ho nth eweigh t givent oth e traitscontaine d inth e life-history tactic.Puttin g thetac ­ ticsalon g ther- K gradient,th e trend ineg gproductio n isgenerall y from high (r-selected)t olo w(K-selected ), bu ta trai tlik ethelytok yma ycaus e someshifts .I nth eR-C- S triangle ther- Kcontinuu m isextende db yth edi ­ mensionstress-toleranc e(S-selection) ;translate di nterm so fmicroarthro - podlife-histor y traits,S-selectio n iscomparabl e tofacultativ e diapause orquiescence ,use d tobridg ehars hpart s of thecycli c period,o r tosea ­ sonal iteroparity thatca nbridg e alos tseason .Trait s likeobligat edia ­ pause or semelparity, however, are not only S-selected, and life-history tactics including these traits are placed in the middle of the triangle, which ispoorl y defined. The quadrant of Southwood (1977)i swel l defined and traits selected for 'later' are diapause or quiescence and seasonal iteroparityan dthos efo r'elsewhere 'ar ephores yan danemochory ,resultin g in the placing of facultative phoretics (II; partially) and facultative diapause with anemochory (VII)i nth e 'later-elsewhere ' section.Althoug h well-defined,th etime-spac equadran tpoorl ydistinguishe sbetwee nsevera l tactics,becaus etrait so ndevelopmen tan dtyp eo rrat eo freproductio nar e not considered. Theschem eo fenvironmenta l characteristics according toStearn s (1976) is filled with the microarthropod life-history tactics (Table 2.3). Stearns' scheme is elaborated in detail for organisms living longer than onecycli cperiod ,bu tdoe sno tdiscriminat eamon gth etactic so forganism s livingshorte r thanth ecycli cperiod .Althoug h developed anddefine ddif ­ ferently,th eschem eo fStearn san dth emicroarthropo dlife-histor y tactics mayb emutuall y supplementary,but ,a sstate d inth esectio no nboundarie s and transitions,th edistinctio nbetwee nunivoltin e andmultivoltin espe ­ cies is subject to critism. Both Stearns'schem e andth epropose d schemeo flife-histor y tacticso f microarthropods,ar emulti-dimensiona lan dthu shar dt ovisualiz eentirely . Figure 2.5 shows the interrelationships of the life-history tactics of

39 Microarthropod communities

r IV III VIII XII II XI X K selected VII VI V lb la IX selected

now later

here la, IX, X, XI V, VI. VIM. XII

elsewhere lb. •1 , III. IV II. VII

Figure 2.6. Projection of microarthropod life-history tactics on a) the r-K continuum of MacArthur and Wilson (1967), b) the C-S-R triangle of Grime (1977), and c) the time-space quadrant of Southwood (1977). See Table 2.1 for definition of the life-history tactics.

40 Life-history tactics

Table 2.3. Environmental conditions according to Stearns (1976)wit h allocated micro-arthropod life-history tactics.

Environmental conditions Life-history tactics

1 Cyclic, fixed period I, II,VI ,VII ,VIII , X, XI period > > life span

2 Cyclic, fixed period period < life span: a. start of cycle and conditions V during cycle predictably favourable b. start of cycle predictable within IX limits, cycle predictably favourable c. start of cycle predictable,condi ­ XII tions during cycle unpredictable; no information on future conditions available at start of cycle d. as c,bu t some information available on future conditions

3 not cyclic, distributed randomly III, IV over time. microarthropods.Fro mth ecentrall yplace dsexua lreproductio n(tacti cXI) , twomai n groups of tactics diverge,tactic swit hphores y and thosewit h a diapause form (including quiescence), aswel l as twomino r groups oftac ­ tics, those with seasonal iteroparity and thelytoky. Further subdivision of the group having diapause forms, discriminates between tactics with semelparity or anemochory. Groups with phoresy canb e divided into those with zoobiontic tactics and obligate phoresy. The scheme isno t intended to imply phylogenetic relationships.

RELEVANCE TO OTHER ORGANISMS

An interestingpoin t isth egeneralit y ofth elife-histor y traitso nwhic h thetactic s arebased .Diapaus e forms (orquiescence )ar ewidesprea d among insects. In plants the equivalent traits may be seed dormancy and the persistence of seed banks,nex t to phanerophyte and geophyte life forms. Anemochoryi sals ocommo ni nman yinsect sa swel la si nplants .Directiona l migration, or phoresy, may be equated with myrmecochory, endozoochory in plantswit hobligat ephores y (oftennecessar y forgermination )an dexozoo -

41 Microarthropod communities chorywit hfacultativ ephoresy .Thelytok y andarrhenotok y areno tuncommo n amonginsects ;thelytok yoccurs ,e.g. , inwhit eflie san daphid s (Homopte- ra:Aphidin aan dfe wAleyrodina) , inbraconi dwasp s (Hymenoptera;Braconi - dae), an d in several beetles (Coleoptera; Staphylinidae,Curculionidae) , arrhenotoky insevera lHymenoptera .Thelytok y alsooccur s insevera lothe r invertebrates such as earthworms (Edwards & Lofty 1972), isopods (Sutton 1972)an dnematode s (Bongers 1988).Th evegetativ e reproduction ofplant s may be compared with apomictic thelytoky and cleistogamy with automictic thelytoky.Vlvipary , seena sparenta lcar e inmicroarthropods ,ma yb ecom ­ paredwit h stolon or rhizome production inplants . Thus, the life-history traitsuse d inth e definition of microarthropod life-history tactics are of general importance (or can be translated to equivalent traits), soa definitio no f the same tacticsusin g otherorga ­ nismsma yb e possible. However,no t all tactics are likely tohav erepre ­ sentatives among allkind s oforganisms ,an dne w tactics alsoma yhav e to be defined insituation swher e examples frommicroarthropod s are lacking, such as thelytoky with aseasonall y initiated sexual generation, found in cladocerans (Ruvinsky et al. 1978) and aphids (Heie 1980), or thelytoky with aseasonall y initiated arrhenotokous reproduction inrotifer s (Allan 1976).

DISCUSSION

The traits onwhic h thelife-histor y tacticsar ebased , presented inthi s paper,ar eno tentirel ydiscrete .Eve na seemingl ydiscret edifferenc esuc h asbetwee n sexual reproduction and thelytoky is continuous, if seen on a large scale as in geographic parthenogenesis, or on a smaller scale as environmentally induced female-biased sex ratios. Suomalainen (1950) and Glesener & Tilman (1978)hav e reviewed geographic parthenogenesis. They concluded that thelytoky occurs at high rather than low latitudes and altitudes, inxeri c rather than mesic biotopes, in disturbed rather than undisturbed places ando n islands rather thano n themainland . Glesener & Tilman (1978)showe d that thecos to fmeiosi si sexplaine db y thebiologi ­ cal uncertainty individuals have to cope with.A s thebiologica l stress, either a generation later,o r ina ne wbiotope , isuncertain , somevaria ­ tioncreate db youtcrossin g isfavourable .Thi simplie stha tth ebiologica l uncertainty increases forcompetitor so fa sexua lspecies ,an dhence ,the y should alsob e sexual.I n thiswa y sexual reproduction isa self-maintai­ ning traita slon ga sbiologica l interactionspla y aprominen t role.Muta ­ tismutandis , inbiotope swher e that role isles s effective,du e tohars h conditions (highaltitude san dlatitudes ,xeri cbiotopes) ,o rt o isolation

42 Life-history tactics

(islands), asexual reproduction isfavoured . Insuc hplaces ,whe npopula ­ tiondensit y iscomparativel y low andmate-findin g thusma yb e difficult, thelytokyha sa nadditiona ladvantag e (Gerritsen1980) .Ofte nasexuall yre ­ producingspecie sar epolyploid ,whic hi sconsidere dt ohav eextr aadaptiv e value,especiall yunde rhars hcondition s (e.g.Suomalaine n 1962).Polyplo ­ idyi spredominantl y associatedwit hapomicti c thelytoky.Tw o tacticswer e defined forthelytokou s species (IXan d X), one (IX)contain s specieswit h seasonaliteroparit yan dthelytoky .Seasona literoparit y issee na sa trai t to overcome years of low reproduction. Murdoch (1966) showed that in the carabidbeetl e Agonum fuliginosum therewa sa ninvers erelationshi pbetwee n reproductionan dsurvival :individual swhic hcoul dno treproduce ,o rhardl y reproduced,du et ounfavourabl econditions ,ha da bette rchanc eo fsurviva l and reproduction in thenex t season. In specieswit hbot h thelytokous and sexual forms (geographic parthenogenesis,Suomalainen , 1950), acontinuu m canb e expected. Inautomicti c thelytoky, indications of the existence of intermediatesar epresen t inth efor mo fatavi cmale s (Taberly 1988). These genuine males produce a few spermatophores but dono t seem topla y arol e inreproduction ,becaus e thethelytokou s femalesd ono tpic ku pth esperma ­ tophores. A trend in sexually reproducing species is given by Trivers & Willard (1973) stating that food shortage or other environmental stress mightselec tfo rth eproductio no ffemal eoffspring .Selectio nfo rth epro ­ ductiono f eithermale s or females isshow nb y Starzyk& Witkowsk i (1986) incerambyci dbeetles .Thus , thelytoky inhars henvironment s canb e either automictic,th een do fa ,possibl ycontinuous ,shif ti nsex-ratio ,o rapo ­ mictic,wit hpolyploid yver yprobable .Thi sresult si ntw oway so fmaintai ­ ning some genetic variationwithou t mating. Insexua l species,th e effect ofa female-biased sex-ratio due tohars h environmental conditionsma yb e equivalent to that of automictic thelytoky. Seasonal iteroparity is also associated with species living under harsh conditions.

Other traits form amor e distinct continuum. Diapause in its obligate form can be seen as the adaptational end of a continuum that runs from quiescencevi afacultativ ediapause .Th econtinuu mo fphoresy ,runnin gfro m accidental,vi afacultative ,eithe rt oobligat ecarrier-unspecifi cphores y (witho rwithou tspecia ladaptations) ,o rt oobligat ecarrier-specifi cpho­ resyfinall y ends inparasitism , aspointe d outi nth esectio no nobligat e and facultative phoresy and carrier-specificity. Borderline species may give rise tosom edifficultie s inth e practical use of the system of life-history tactics,whic h is a general problem of classification.Althoug h all classificationshav e theirborderlin ecases , itma yb econclude dtha tth epresen tclassificatio no flife-histor y tactics of microarthropods is based on well-defined, determinable life-history traits. The defined tactics and the component life-history traits may be applicable for other higher taxa thanmicroarthropods .

43 Microarthropod communities

REFERENCES

Allan, J.D., 1976. Life-history patterns in zooplankton. American Naturalist 110,165-180 . Athias-Binche, F., 1981. Ecologie desuropodide s édaphiques (Arachnides: Parasitiformes) de trois écosystèmes forestiers. 1. Introduction, material,biologie . Vie Milieu 31,137-147 . Athias-Binche, F., 1984.L a phorésie chez les acariens uropodides (Anactinotriches),un e stratégie écologique originale.Act aOecologia / Oecologia Generalis 5,119-133 . Barra,J.A . &N .Poinsot-Balaguer , 1977.Modification s ultrastructurelles accompagnant l'anhydrobioseche zu ncollembole : Folsomidesvariabilis . Revue d'Ecologie et Biologie du Sol 14,189-197 . Bell,G. ,1976 .O nbreedin gmor etha nonce .America nNaturalis t110 ,57-77 . Bhattacharya, T., V.C. Joy & S. Joy, 1978. Studies on the effect of temperature on the development of Oppia nodosa. Entomon 3,149-155 . Bhattacharyya, S.K., 1963.A revision of the British mites of the genus Pergamasus Berlese s. lat. (Acari: Mesostigmata). Bulletin British Museum (Natural History) 11,133-242 . Binns, E.S., 1972. Arctoseius cetratus (Sellnick) (Acarina: Ascidae) phoretic onmushroo m sciarid flies.Acarologi a 14,350-356 . Binns, E.S., 1973. Digamasellus fallax Leitner phoretic on mushroom sciarid flies.Acarologi a 15, 10-17. Binns, E.S.,1974 .Note s on thebiolog y ofArctoseiu s cetratus (Sellnick) (Mesostigmata: Ascidae). Acarologia 16,577-582 . Binns, E.S., 1982. Phoresy as migration - some functional aspects of phoresy inmites .Biologica l Review 57,571-620 . Blancquaert,J.-P. ,R . Coessens &J . Mertens, 1981.Lif e history of some Symphypleona (Collembola)unde r experimental conditions. I. Embryonal development and diapause. Revue d'Ecologie et Biologie du Sol 18, 115-126. Bongers, T., 1988. De nematoden van Nederland. Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging, Utrecht,40 8p . Charnov, E.L. &W.M . Schaffer, 1973.Lif ehistor y consequences of natural selection: Cole's result revisited. American Naturalist 107,791-793 . Chen, C.N., C.C. Cheng & K.C. Hsiao, 1979. Bionomics of Steneotarsonemus spinki attacking rice plants in Taiwan. In: Rodriguez, J.G. (ed.), Recentadvantage s inacarology .Academi cPress ,Ne wYork .Vol .I. ,111 - 117. Chmielewski,W. , 1970.Th e passage of mites through the alimentary canal ofvertebrates . Ekologia Polska 35,741-756 . Cole, L.C., 1954.Th e population consequences of life history phenomena. Quarterly Review of Biology 29,103-137 . Davidson, J., 1934. The 'Lucerne flea' Sminthurus viridis L. Collembola inAustralia . Bulletin Councel for Scientific and Industrial Research (Melbourne) 79, 1-66. Desender, K. & M. Vaneechoutte, 1984. Phoretic associations of carabid beetles (Coleoptera, Carabidae) andmite s (Acari). Revue d'Ecolgie et Biologie du Sol 21,363-371 . Edwards, C.A. & J.R. Lofty, 1972. Biology of earthworms. Chapman & Hall,

44 Life-history tactics

London, 283p . Farish, D.J. & R.C. Axtell, 1971. Phoresy redefined and examined in Macrocheles muscadomesticae (Acarina: Macrochelidae).Acarologi a 13, 16-29. Fashing, N.J., 1975. Life history and general biology of Naiadacarus arboricola Fashing,a mit e inhabitingwater-fille d treeholes (Acarina: Acaridae). Journal ofNatura l History 9,413-424 . Fashing, N.J., 1979.Naiadacaru s arboricola, a 'K-selected' acarid mite. In: Rodriguez, J.G. (ed.), Recent advantages in acarology. Academic Press, New York. Vol. I., 525-529. Gerritsen, J., 1980. Sex and parthenogenesis in sparse populations. American Naturalist 115,718-742 . Glesener, R.R. & D. Tilman, 1978. Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals.America n Naturalist 112,659-673 . Grandjean, F., 1941. Statistique sexuelle et parthénogenèse chez les Oribates (Acariens). Compte rendu hebdomadaire Séance Académie Scientifique Paris,212 ,463-467 . Greenslade, P.J.M., 1983. Adversity selection and the habitat templet. American Naturalist 122,352-365 . Greenwood, P.J. & J. Adams, 1987. The ecology of sex. Edward Arnold, London. Griffiths, D.A., 1964. Experimental studies on the systematics of the genus Acarus Linnaeus 1758. (Sarcoptiformes, Acarina). Acarologia 6, fascimile hors series,101-116 . Grime,J.P. , 1977.Evidenc e for theexistenc e of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169-1194. Grime, J.P., 1979. Plant strategies and vegetation processes. John Wiley & Sons, New York. Grime,J.P. ,J.G . Hodgson & R. Hunt, 1988.Comparativ e plant ecology. A functional approach to common British species.Unwi n Hyman, London. Hale, W.G., 1965a. Observations on thebreedin g biology of Collembola. Pedobiologia 5, 146-152,161-177 . Hale, W.G., 1965b. Post-embryonic development in some species in Collembola. Pedobiologia 5,228-243 . Harvey, P.H. & M.P. Pagel, 1991. The comparative method in evolutionary biology. Oxford University Press,Oxford , UK. Heie, O.E., 1980.Th eAphidoide a (Hemiptera)o fFennoscandi a and Denmark. I. Fauna Entomologica Scandinavica Vol. 9. Scandinavian Science Press Ltd, Klampenborg, Denmark. Helle,W. , 1965.Populatio n genetics ofarrhenotokou s mites.Bolletin o di Zoologia Agraria e Bachicoltora Ser. II. 7,219-225 . Helle, W. & H.R. Bolland, 1967. Karyotypes and sex determination in spider mites.Genetic a 38,43-53 . Hughes, A.M., 1976. The mites of stored food and houses. Technical Bulletin 9, Ministry ofAgriculture , Fisheries and Food, London. Hunter, P.E. & R.M.T. Rosario, 1988. Associations of Mesostigmata with other arthropods.Annua l Review of Entomology 33,393-417 . Hutson, B.R., 1978. Influence of pH, temperature and salinity on the fecundityan dlongevit yo ffou rspecie so fCollembola .Pedobiologi a18 ,

45 Microarthropod communities

163-179. JalilM . &J.G . Rodriguez, 1970. Studies ofbehaviou r ofMacrochele s muscadomesticae (Acarina: Macrochelidae) with emphasis on its atraction to the house fly. Annals of the Entomological Society of America 63,738-744 . Janssen, G.M. & E.N.G. Joosse, 1987. Reproduction and growth in Collembola under laboratory conditions. Pedobiologia 30,1-8 . Jeppson, L.R., H.H. Keifer & E.W. Baker, 1975. Mites injurious to economic plants.Universit y of California Press, Berkeley. Joosse, E.N.G., 1969. Population structure of some surface dwelling Collembola ina coniferou s forestsoil .Netherland sJourna lo fZoolog y 19, 621-634. Joosse, E.N.G., 1983.Ne w developments in the ecology ofApterygota . Pedobiologia 25,217-234 . Joosse, E.N.G. & E.Veltkamp , 1970.Som e aspects of growth, moulting and reproduction in five species of surface dwelling Collembola. Netherlands Journal of Zoology 20,315-328 . Joosse, E.N.G. & H.A. Verhoef, 1974. On the aggregational habits of surface dwelling Collembola. Pedobiologia 14,245-249 . Karg, W., 1971.Acar i (Acarina), Milben Unterordnung Anactinochaeta (Parasitiformes), Die freilebenden Gamasina (Gamasides), Raubmilben. Die Tierwelt deutschlands 59,Gusta v Fischer Verlag, Jena. Karg,W. , 1989.Acar i (Acarina), MilbenUnterordnun g Parasitiformes (Anactinochaeta)Uropodin aKramer ,Schildkroetchenmilben . DieTierwel t deutschlands 67,Gusta v Fischer Verlag,Jena . Karl, E., 1965a. Untersuchungen zur Morphologie und Oekologie von Tarsonemiden gaertnerischen Kulturpflanzen. I. Tarsonemus pallidus Banks. Biologisches Zentralblatt 84,47-80 . Karl, E., 1965b. Untersuchungen zur Morphologie und Oekologie von Tarsonemiden gaertnerischen Kulturpflanzen. II. Hemitarsonemus latus (Banks),Tarsonemu sconfusu sEwing ,T .talpa eSchaarSchmidt ,T .setife r Ewing, T. smithi Ewing und Tarsonemoides belemnitoides Weis-Fogh. Biologisches Zentralblatt 84,331-357 . Krantz, G.W. & J.O. Whitaker, 1988. Mites of the genus Macrocheles (Acari:Macrochelidae )associate dwit h smallmammal s inNort hAmerica . Acarologia 29,225-259 . Krczal, H., 1959 . Systematiek und Oekologie der Pyemotiden. Beiträge zur Systematikun dOekologi emitteleuropäische r Acarina1 ,Abschn . 3,385 - 625. Lindquist, E.E., 1969.Revie w ofholarcti c tarsonemid mites (Acarina: Prostigmata) parasitizing eggs of ipine bark beetles. Memoirs of the Entomological Society of Canada 60,1-111 . Lindquist,E.E. ,1975 .Association s betweenmite s and other arthropods in forest floor habitats. Canadian Entomologist 107,425-437 . Lindquist, E.E., 1986. The world genera of Tarsonemidae (Acari: Hetero­ stigmata):a morphological ,phylogenetic ,an dsystemati crevision ,wit h areclassificatio no ffamily-grou p taxai nth eHeterostigmata . Memoirs of the Entomological Society of Canada 136, 1-517. Lindquist, E.E.& W.D . Bedard, 1961.Biolog y and taxonomy ofmite s of the genus Tarsonemoides (Acarina: Tarsonemidae)parasitizin g eggs ofbar k beetles of the genus Ips. Canadian Entomologist 93,982-999 .

46 Life-history tactics

Luxton, M., 1981. Studies on the oribatld mites of a Danish beech wood soil. IV. Developmental biology. Pedobiologia 21,312-340 . MacArthur, R.H. & E.O. Wilson, 1967.Th e theory of island biogeography. Princeton University Press,Princeton , N.J. McNulty, B.J., 1971. An introduction to the study of acari-insect associations.Proceeding so fth eBritis hEntomologica lNatura lHistor y Society 4, 45-70. Mertens, J., R. Coessens & J.P. Blancquaert, 1983. Reproduction and development of Hypogastrura viatica (Collembola) in relation to temperature and submerged conditions. Revue d'Ecolgie et Biologie du Sol 20,567-577 . Metz, L.J., 1971.Vertica l movement ofAcarin a under moisture gradients. Pedobiologia 11,262-268 . Mitchell, R., 1970. An analysis of dispersal in mites. American Naturalist 104,425-431 . Murdoch, W.W., 1966. Population stability and life-history phenomena. American Naturalist 100, 5-11. Najt, J., 1983. Modifications morphologiques liées à 1'écomorphose chez les collemboles Isotomidae. Pedobiologia 25,337-348 . Nannelli, R., 1975. Osservazioni sulla biologia di Oppia concolor in condizioni sperimentali di allevamento. Redia 56,11-116 . Niijima, K., 1973. Experimental studies on the life history, fecundity andgrowt ho fSinell acurviset a (Apterygota,Collembola) . Pedobiologia 13, 186-204. Norton, R.A., 1980. Observations on phoresy by oribatid mites (Acari: Oribatei). International Journal ofAcarolog y 6, 121-130. Nutting, W.B., 1964.Demodicida e -statu s and prognostics.Acarologi a 6, 441-454. Oliver Jr, J.H., K. Tanaka & M. Sawada, 1973. Cytogenetics of ticks (Acari: Ixodoidea) 12. Chromosomes and hybridization studies of bisexualan dparthenogeneti cHaemaphysali slongicorni srace sfro mJapa n and Korea. Chromosoma 42,269-288 . Palmer, S.C. & R.A. Norton, 1990. Further experimental proof of thelytokous parthenogenesis in oribatid mites (Acari: Oribatida: Desmonomata). Experimental and Applied Acarology 8,149-159 . Pereira, C.& M.P .d e Castro,1947 .Fores e eparthénogenès e arrenotoca em Macrocheles muscadomesticae (Scopoli) (Acarina,Macrochelidae ) e suan gisifacaoecologica .Archivo s Instituto Biologico SaoPaul o 18,71-89 . Petersen,H. , 1980.Populatio n dynamic and metabolic characterization of Collembola species ina beec h forest ecosystem. In:Dindal ,D.L . (ed.) Soil biology as related to land use practices. Proceedings VII. International SoilZoolog y Colloquium ofth eI.S.S.S. , Syracuse,N.Y. , 806-833. Ruvinsky, A.O., S.F. Cellarius & Yu. G. Cellarius, 1978. The possible role of genome activity changes in the sex determination of Daphnia pulex. Theoretical andApplie d Genetics 52,269-271 . Schaarschmidt, L., 1959. Systematik und Oekologie der Tarsonemlden. Beiträge zur Systematik und Oekologie mitteleuropäischer Acarina 1, Abschnitt 5,713-823 . Scheucher, R., 1959. Systematik und Oekologie der deutschen Anoetinen. Beiträge zur Systematik und Oekologie mitteleuropäischer Acarina 1,

47 Microarthropod communities

Abschnitt 2,233-384 . Sharma, G.D. & D.K.McE. Kevan, 1963.Observation s on Folsomia similis (Collembola: Isotomidae) in Eastern Canada. Pedobiologia 3, 48-61. Skaife, S.H., 1952. The yellow-banded carpenter bee, Mesotrichia caffra Linn., and its symbiontic mite,Dinogamasu s braunsiVitzthum . Journal of the Entomological Society of South Africa 15,63-76 . Snider, R.J., 1983.Observation s on the oviposition, egg development and fecundity of Onychiurus (Onychiurus) folsomi at constant temperature. Pedobiologia 25,241-252 . Somme, L., 1981. Cold tolerance of alpine, arctic, and antarctic Collembola and mites. Cryobiology 18,212-220 . Southwood, T.R.E., 1962.Migratio n of terrestrial arthropods in relation tohabitat . Biological Reviews 37,171-214 . Southwood, T.R.E., 1977.Habitat , the templet for ecological strategies? Journal ofAnima l Ecology 46,337-365 . Southwood,T.R.E. ,1988 .Tactics ,strategie san dtemplets .Oiko s 52,3-18 . Springett, B.P., 1968. Aspects of the relationship between hurrying beetles,Necrophoru s spp. and themit e Poecilochirus necrophori Vitz. Journal ofAnima l Ecology 37,417-424 . Starzyk, J.R. & Z. Witkowski, 1986. Dependence of the sex-ratio of cerambycid beetles (Col., Cerambycidae) on the size of their host trees. Journal ofApplie d Entomology 101,140-146 . Stearns, S.C., 1976. Life-history tactics: a review of the ideas. Quarterly Review Biology 51, 3-47. Stearns, S.C., 1992. The evolution of life histories. Oxford University Press, Oxford, UK. Stefaniak, 0. & S. Seniczak, 1981. The effect of fungal diet on the development ofOppi aniten s (Acari,Oribatei )an do nth emicroflor a of its alimentary tract. Pedobiologia 21,202-210 . Suomalainen, E., 1950. Parthenogenesis in animals. Advances in Genetics 3,193-253 . Suomalainen, E., 1962 . Significance of parthenogenesis in the evolution of insects.Annua l Review of Entomology 7,349-366 . Sutton, S.L., 1972.Woodlice . Ginn & Company, London, 144p . Sweatman, G.K., 1971. Mites and pentastomes. In: Davis, J.W. & R.C. Anderson (eds) Parasitic diseases of wild mammals. Iowa State University Press,Ames , Iowa,U.S.A. , 3-64. Taberly, G., 1987a. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). I.Acarologi a 28,187-198 . Taberly, G., 1987b. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). III. Etude anatomique, histologique et cytologique des femelles parthénogénétiques. Acarologia 28,389-403 . Taberly, G., 1988. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribates: Trhypochthonius tectorum (Berlese) et Platynothruspeltife r (Koch).IV .Observation ssu rle smâle sataviques . Acarologia 29, 95-107. Tamm, J.C., 1984. Surviving long submergence in the egg stage - a successful strategy of terrestrial arthropods living on flood plains (Collembola, Acari, Diptera). Oecologia 61,417-419 .

48 Life-history tactics

Tanigoshi, L.K. & J.A. Logan, 1979. Tetranychid development under variable temperature regimes. In: Rodriguez, J.G. (ed.), Recent advantages in acarology. Academic Press,Ne w York. Vol. I., 165-175. Tauber, M.J., CA. Tauber & S. Masaki, 1986. Seasonal adaptations of insects. Oxford University Press,Ne wYork . Travé, J. & F. Duran, 1971.Développemen t et comportement en laboratoire de Neoribates gracilis.Vi e Milieu 22,79-89 . Trivers,R.L . &D.E .Willard , 1973.Natura l selection ofparenta l ability tovar y the sex ratio of offspring. Science 179, 90-91. Van der Hammen, L., 1972.Spinachtigen , Arachnidea. IV.Mijten ,Acarida . Algemene inleiding in de acarologie. Koninklijke Nederlandse Natuur­ historischeVereniging ,Wetenschappelijk eMededelin g91 .Hoogwoud ,Th e Netherlands. Van Eyndhoven,G.L. , 1964.Cheleytomorph a lepidopterum (Shaw,1794 ) (-Ch. venustissima) (Acari, Cheleytidae) on Lepidoptera. Beaufortia 11, 53-60. Van Straalen, N.M. & E.N.G. Joosse, 1985. Temperature responses of egg production and egg development in two species of Collembola. Pedobiologia 28,265-278 . Wade, C.F. & J.G. Rodriguez, 1961. Life history of Macrocheles muscado- mesticae (Acarina:Macrochelidae ) ,a predato ro fth ehous efly .Annal s of the Entomological Society ofAmeric a 54,776-781 . Wallace, M.M.H., 1970a. Diapause in the aestivating egg of Halotydeus destructor. Australian Journal of Zoology 18,295-313 . Walter, D.E., H.W. Hunt & E.T. Elliott, 1987.Th e influence of prey type on the development and reproduction of some predatory soil mites. Pedobiologia 30,419-424 . Walter, D.E. & D.T. Kaplan, 1990. A guild of thelytokous mites (Acari: Mesostigmata) associated with citrus roots in Florida. Environmental Entomology 19,1338-1343 . Walter, D.E. &J.H . OliverJr , 1989.Geolaelap s oreithyiae n. sp. (Acari; Laelapidae), a thelytokous predator of arthropods and nematodes, and adiscussio no fclona lreproductio ni nth eMesostigmata .Acarologi a30 , 293-303. Webb, N.R., 1977. Observations on Steganacarus magnus. General biology and life cycle.Acarologi a 19,686-696 . Williams, G.C., 1975. Sex and evolution. Princeton University Press, Princeton New Jersey. Witteveen, J. & E.N.G. Joosse, 1987. Growth, reproduction and mortality in marine littoral Collembola at different salinities. Ecological Entomology 12,459-469 . Woodring, J.P. & E.F. Cook, 1962. The biology of Ceratozetes cisalpinus Berlese,Scheloribate s laevigatusKoch ,an dOppi aneerlandic a Oudemans (Oribatei), with a description of all stages.Acarologi a 4, 101-136. Wrensch, D.L., J.B. Kethley & R.A. Norton, 1994. Cytogenetics of holokinetic chromosomes and invertedmeiosis :key s toth e evolutionary success ofmites ,wit h generalizations oneukaryotes . In:Houck ,M.A . (ed.) Mites: ecological and evolutionary analysis of life-history patterns, pp 282-343. Young, S.R. & W. Block, 1980. Experimental studies on the cold tolerance ofAlaskozete s antarcticus. Journal of Insect Physiology 26,189-200 .

49 Microarthropod communities

Zachvatkin,A.A. , 1959. Fauna of the U.S.S.R. Arachnoidea 6 (1)Tyrogly - phoidea. American Institute of Biological Sciences,Washington .

50 Applications of microarthropod life-history tactics in

nature management and ecotoxicology

SUMMARY. Thepractica lus eo fmicroarthropo dlife-histor ytactic si nnatur e management andecotoxicolog y isdemonstrated .A ke y toth e tactics ispre ­ sented to facilitate the use of the life-history tactics. Examples are giveno fth edistributio nove r these tacticso fmicroarthropod sfro ma fo ­ rest, agrassland , anda sal tmarsh .Th eproces s ofdecompositio no fgras s leaves in litterbags is illustrated using life-history tactic diagrams. Effects of various disturbances can be well documented by shifts in the distribution of life-history tactics of species. Irregular unpredictable disturbances leadt oa nincrease d representationo fphores y tactics.Regu ­ lar disturbances lead to an increased representation of synchronization tactics.Permanen tan dpersisten tpollution ,finally ,lead st oa nincrease d representation oftactic swit h thelytokous reproduction. The consequences ofth elatte r forecotoxicolog y arediscussed . Iti sconclude d thatmicro ­ arthropod life-history tactics meet the formerly described criteria per­ mitting comparisons between effects of management measures and pollution indifferen t biotopes andcountries .

INTRODUCTION

InChapte r 2I followe d Stearns (1976)i ndefinin g life-history tacticsa s co-adaptedset so fmeaningfu llife-histor ytraits .A classificatio no ftac ­ ticswa sprimaril y based onpropertie s ofmicroarthropods ,bu t thecompo ­ sing traits are general and widespread in all kinds of organisms. This classificationi sals osuppose d tohav ea mor egenera lvalu ean di ti smor e differentiated than previous ones (MacArthur & Wilson 1967;Grim e 1977, 1979; Southwood 1977,1988 ;Stearn s 1976;Hol m 1988). The objective of this chapter is to apply this classification in eco­ toxicology and nature management. An identification key is presented to improveth e accessibility ofth e life-history tacticso fmicroarthropods .

51 Microarthropod communities

Severalexample sar epresente dt oillustrat etha tth esyste mo flife-histo ­ rytactic smeet s theadvantage s sensu Grimee t al. (1988): allowingcompa ­ risonsbetwee nbiotopes ,countrie s andeffect s ofdifferen t environmental impacts. Sixhypothese sembracin gal lthre emajo rgroup so flife-histor ytactics , i.e. reproduction tactics,synchronizatio n tactics,an ddispersa l tactics (Chapter 2),ar e tested. (1)I nrelativel yundisturbe decosystem s specializedtactic sar euncom ­ mon among microarthropods. (2)Durin g the process of decomposition of Avenella leaves in litter- bags, initially an increase of fastcolonizer s (dispersal tactics) isex ­ pected,wherea s in later stages species adapted tomor e constant environ­ ments may take over (tactics with thelytoky). Indisturbe d ecosystems, (3) such as cattle-grazed (a small-amplitude irregular disturbance) versus ungrazed grasslands, and (4)suc h ashigh - productiongrassland swit hintensiv emanagemen t (ahigh-amplitud e irregular disturbance)versu s semi-natural grasslands,a comparativel yhighe r frac­ tion of dispersal tactics and a lower fraction of tactics with thelytoky is expected in the disturbed grasslands. (5)I n situations with amor e regular disturbance, such as the fluctu­ ationo fth ewaterleve l ina storag e reservoiraffectin g themit e faunao n annuallydraine dfloo dplains ,a relativ e increaseo fsynchronizatio ntac ­ tics isexpected .Wit h increasingdept h insuc ha storag ereservoi runcer ­ tainty about submergence increases and only species best adapted to such conditions reach high densities. (6)I nbiotope s with apersisten t pollutionb yheav y metals orpersis ­ tent insecticides,th econstanc y ofthi spollutio nma y leadt oa n increase ofmicroarthropo dlife-histor ytactic swit hthelytoky .Nex tt opredictable , such abiotop eha sbecom e ahars h environment,wher e species interactions presumably play amino r role, so sexual reproductionma y be less favoured (Glesener and Tilman 1978, Chapter2) .

52 Applications of tactics

MATERIALS ANDMETHOD S

Allocationo fa specie s toa life-histor y tactic isdon e using theke yi n Appendix3.1 .Dataset so fmicroarthropod suse dar epartl yfro mliterature, partly from ownmateria l (Siepel 1990). Only datasets on microarthropods identifiedt oth especie s levelwer eused ,becaus e inorders ,familie san d evengener aseveral ,tactic sca noccur .Furthermore ,dataset sshoul dprefer ­ ablyno tb e limited toon eorde r ofmicroarthropod s only,becaus eno tal l tactics occur ineac h order. For the dominant species in the datasets references will be given to support the identification of their life-history tactics. A species is called dominant when itsnumbe r exceeds 5%o fth etota l number ofmicro ­ arthropods in the sample. If data for a species are missing, the pre­ dominant life-history traits insoi lmicroarthropod s arepresumed : sexual reproduction, iteroparous oviposition,n ophores yan dn o synchronization, resulting intacti cXI .Therefore ,n oconclusion s canb edraw no nchange s in this tactic. All conclusions will be based on positively identified tactics.

RESULTS

Relatively undisturbed ecosystems

Thedistributio no fth emicroarthropod s (Acarian dCollembola )amon glife - history tactics ispresente d fora forest soil using data ofVa nd e Bund and Eijsackers (1986), a grassland soil using data of Siepel andVa nd e Bund (1988) ("BovenbuurtB" )an da sal tmars h usingdat a ofLuxto n (1967) ("Puccinellietum series") (Table3.1) . Thedominan t specieso fth efores tsoi lwere :Platvnothru speltife r (C.L.Koc h 1844),a long-livin g thelytokous species (Taberly 1987): tactic IX;Tectocepheu s velatus (Michael 1880)an dOppiell anov a (Oudemans 1902),bot hiteroparou sthelytokou sspecie s (Grandjean1941 ;Woodin g& Coo k 1962):tacti cX ; Atropacarusstriculu s (C.L.Koc h1836 )a niteroparou ssexuall yreproducin g species:tacti cXI .Non eo f theseoribati d speciesi sknow nt ob ephoreti co rt ohav ea diapause ,whic h alsohold sfo rth esexuall y reproducing mesostigroatidmit e Pergamasusvagabundu sKar g 1966 (Karg 1971): tacticXI . Thedominan tspecie si nth egrasslan dsoi lare :Microppi aminu s(Paol i1908) ,a thelytokousl yrepro ­ ducingshort-livin gspecie s(Luxto n1981 ;Taberl y 1987):tacti cX ;Brachvchthoniu sbimaculatu sWillman n 1936 andSellnickochthoniu s imnaculatus (Forsslund 1942), species assumed tob esexuall y reproducing by analogyt oth erelate d Eobrachvchthonius oudemansiVa nde rHamme n 1952(Wes t 1982): tacticXI .Th e listedoribati dmite sd ono thav ea diapaus eo rphoreti cbehaviour ,whic h alsohold sfo rth esexuall y reproducing collembolanFolsomi a quadrioculata (Tullberg 1871)(Gregoire-Wib o 1974): tacticXI . Thedominan t specieso fth esal tmars har eth eoribatid s Punctoribates quadrivertex (Halbert1920 ) and Hygroribates schneideri (Oudemans 1905), both sexually reproducing species (Luxton 1966): tactic XI. Thesexuall y reproducingmesostigmati dmit eHalolaelap snodosu sWillman n 1952(Kar g1971 )an dth e actinedid speciesCheylostigmaeu s scutatus (Halbert)hav e afacultativ e eggrestin g stage thelatte r by analogy toth erelate dC .pannonlcu s (Willjnann)(Tam m 1984): tactic VIII.

53 Microarthropod communities

Table 3.1. Percentages of individuals per life-history tactic of the microarthropod community of a forest soil, a grassland soil and a salt marsh zone;n is the total number of individuals, s the total number of species observed.

Life history Forest Grassland Salt marsh tactic soil soil zone

I 0 0 0 II 1.99 3.04 7.55 III 0.83 0.78 4.01 IV 0.03 0.37 0 V 0.21 3.23 2.39 VI 0 0 0 VII 0 0.02 0 VIII 0 0 7.42 IX 7.94 0 0 X 15.40 11.95 0 XI 71.87 80.60 78.62 XII 1.53 0.02 0 n 3863 6185 2966 s 72 93 20

The salt marsh compared to both the forest and the grassland soil has norepresentative swit ha thelytokou sreproductio n (tacticsI Xan dX ),bu t hasrepresentative so ftacti cVIII ,facultativ ediapaus eo rquiescence .Th e grassland soil compared to the forest soil lacks long-living thelytokous species (tactic IX), andscore sa littl ehighe ro nth efractio no ffaculta ­ tivephoreti cspecies .Thes edat asugges tincreasin genvironmenta ldynamic s inth esequenc e forestsoi l -grasslan d soil -sal tmars hzone .Th e results areconsisten twit hth efirs thypothesis :specialize dtactic sar erelative ­ lyuncommo n inundisturbe d ecosystems,althoug h thefraction so fdispersa l (II, III, IV) and synchronization tactics (V,VI ,VII ,VIII ) in the salt marshma yb eunderestimated ,becaus elittl elife-histor yinformatio nexist s on the majority of the salt marsh species.

Changes during decomposition in litterbags

Thelife-histor ytactic so fmicroarthropod soccurrin gdurin gth edecomposi ­ tion of leaves of the grass Avenella flexuosa (L.) Dreyer in litterbags placed between litter and mineral soil are presented in Figure 3.1. Data concern a total of 17,695 individuals (eight sampling dates and initial soil microarthropod community together) and 135 species (Siepel, 1990).

54 Applications oftactic s

IMBOS soil community litterbags after 1 month litterbags after 3 months

Figure 3.1. Life-history tactics of microarthropods (mites and spring- tails) during decomposition of leaves of Avenellaflexuos a in litterbags placed between litter and mineral soil. Data from Siepel (1990).

55 Microarthropod communities

Dominant species in any of the sampling periods were: the collerobolans HvpoRastrura denticulata Bagnall1941 ,a relativel yshort-livin gsexuall yreproducin gspecie s (Hale1965) :tacti cXI ;Onvchiuru s furcifer(Borne r1901 )a sexuall yreproducin gspecie s (Hale1965) :tacti cX Ian dOnychiuru ss-vontoerne i (Gisin 1957), assumed tohav e sexualreproduction : tactic XI.I nth egenu sOnvchiuru sbot h sexual (0. tricampatusGisi n 1956:Hal e 1964)an dthelytokou s reproduction (0•armatu s (Tullberg 1669):Grégoire - Wibo& Snide r (1983)an d0 .procampatu sGisi n1956 :Hal e1964 )occur ,i nunknow ncase stherefor especie s wereassume dt ob esexuall yreproducing .Isotomiell amino r (Schaffer 1896)i sthelytokousl y reproducing (Petersen 1980):tacti cX .Th esam ehold sfo rTullberRi akrausbauer i (Borner1901 )accordin gt oPeterse n (1971): tactic X. The listed Collembola areno t phoretic nor do theyhav e adiapause . Two species of tarsoneroidswer efoun dt ob edominant .Scutacaru squadranRuIu sPaol i191 1an dPvRmephoru sc fhaarloevi . Members of the Scutacaridae as well as the Pygmephoridae were phoretics (Binns 1982; Desender & Vaneechoutte 1984;Lindquis t 1986),whic hi sassume dt ob efacultativ e forbot hspecies :tacti c II.Th e astigmatidmite sSchwiebe atalp aOudeman s191 6an dSchwiebe alebrun iFai n 1977ar eknow nt ob ephoreti c ashypop i and tob e carrier-unspecific (Karg 1987): tactic III.Th emesostigmati d PerRamasus truncus Schweizer 1961 is not phoretic and sexually reproducing (Karg 1971): tactic XI; Alliphus siculus (Oudemans 1905)i sphoreti c inal llif estage s (Karg 1971): tactic IVan dUropod aminim a (Berlese 1910) isphoreti c (Athias-Binche 1984)an dthelytokousl yreproducin g (Athias-Binche 1981):tacti cII .Fo rth e oribatid mite Sellnickochthonius zelawaiensis (Sellnick 1928)th e same tactic was assumed as forth e congeneric S. immaculatus before: tactic XI. Nothrus silvestris (Nicolet 1855) has a thelytokous reproduction (Grandjean 1941)an d is long-living (Sengbush 1958): tactic IX. Medioppia subpectinata (Oudemans 1900)ha s sexual reproduction and lives relatively short (Luxton 1981): tacticXI . Comparedt oth einitia lsoi lmicroarthropo dcommunit ymor eobligat epho­ retics (tactics IIIan dIV )wer eobserve d inth eearl ystage so fdecomposi ­ tion. Species phoretic inan y life stage (tactic IV) occurred for aver y short period of time; this was the most 'r-selected' tactic recognized (Chapter 2).Somewha t later facultative phoretics (tactic II) increased. Duringth elate rstage so fdecompositio nspecie swit hthelytokou srepro ­ duction (tactics IX and X) increased. So the initial abundant growth of fungi and bacteria was exploited by phoretic species, obligate phoretics rather than facultative phoretics (fungivores, bacteriovores as well as (nematode)predators) . These specieswer e replaced inlate r stages ofde ­ composition, when fungal growth is less abundant, by microarthropods adapted to a rather constant environment. The majority of the species in that stage ofdecompositio n inth e litterbags had a thelytokous reproduc­ tion. The final stage of decomposition did not resemble the initial soil community (Fig. 3.1),becaus e of the location of the litterbags in the stratum between litter andminera l soil. Faunal composition of the final stage resembled the euedaphic faunal community. Theseresult s areconsisten twit h thesecon dhypothesis :a ninitia lin ­ crease of fast colonizers (phoretics) and a relative large fraction of thelytokous species in the late stages of the decomposition process.

The effects of fertilization and cattle grazing

Siepelan dVa nd eBun d (1988)investigate d themicroarthropo d community of threetype so fgrasslands :unfertilized , littlean dheavil y fertilized. In each type, cattle-grazed and mown grasslands were represented. The data showeda shif t inlife-histor y tactics fromunfertilize d toheavil yferti ­ lized grasslands and a difference between mown and cattle-grazed grasslands.

56 Applications of tactics

Dominant species among theOribatid a inan yo fth egrassland swer eBrachychthoniu sbimaculatu san d Sellnickochthoniusimmaculatus :tacti cXI ;Microppi aminu san dTectocepheu svelatus :tacti cX a spointe d out above. Liebstadia similis (Michael 1888), Minunthozetes semirufus CC.L. Koch 1841), Ramusella clavipectinata (Michael 1885) and Achipteria coleoptrata (Linnaeus 1758): tactic XI (Luxton 1981; Sengbush 1958). DominantCollembol awere :HypoRastrur adenticulat a tactic XI aspointe d outabov ean d Frieseamirabili s (Tullberg 1871), Isotomasensibili s (Tullberg 1871), I.viridi s (Bourlet 1839), I. olivacea (Tullberg 1871)an dProisotom aminut a (Tullberg 1871): tacticX I (sexualreproduction ) (Hale 1965), and finally Sminthurinusaureu s (Lubbock 1862): tactic VIII (with a facultative diapause:Va n Straalen et al. 1985). Dominant Tarsonemidawere : Scutacarus quadrangulus: tactic II aspointe d out above,an dPygmephoru smesembrina e(Canestrin i 1881):tacti cII ,facultativ ephores y (Krczal1959) .Th e only dominant mesostigmatidmit e wasDendrolaelap s rectusKar g 1962,whic h is facultatively phoretic (Karg 1971): tacticII . Incattle-graze dcompare dt oungraze dgrasslands ,facultativ e phoretics (tactic II)an dobligat ephoretic s (tactics IIIan dIV )wer emor e abundant (Wilcoxontwo-sampl e test:p<0.025) . Figure 3.2 givespi e diagrams of the life-history tactics found in an ungrazed and a cattle-grazed grassland. Theresul ti sconsisten twit hth ethir dhypothesis :a comparativel y larger fractiono fspecie swit hdispersa l tacticsan da lowe r fractiono fspecie s with thelytoky in the cattle-grazed grasslands. In fertilized grasslands obligate phoretics (tactics III and IV),an d species with facultative diapause or quiescence (tactic VIII) were more abundant thani nunfertilize dgrasslands ,whil ei nunfertilize d grasslands thelytokously reproducing species with or without seasonal iteroparity (tactics IX and X, respectively) were more abundant (Wilcoxon test: p<0.01). Figure 3.3 presents the life-history tactics in an unfertilized anda heavil y fertilized grassland.A sexpecte dfro m thefourt hhypothesi s theheavil yfertilize dgrasslan dha da highe rfractio no fspecie swit hdis ­ persal tactics and alowe r fraction ofspecie swit h thelytokous reproduc­ tion. The differences in this high-amplitude disturbance were more pro­ nounced than in the small-amplitude disturbance of cattle-grazing.

BOVENBUURT C BOVENBUURT S

Figure 3.2. Life-history tactics of microarthropods (mites and spring- tails) from a mown (Bovenbuurt C) and a cattle-grazed grassland (Boven- buurt S) in The Netherlands. Data from Siepel & Van de Bund (1988).

57 Microarthropodcommunitie s

DEELERWOUD DROEVENDAAL

Figure 3.3. Life-history tactics of microarthropods (mites and springtails) from an unfertilized (Deelerwoud) and a highly fertilized grassland (Droe- vendaal: 400 kg N ha~1yr'x) in The Netherlands. Data from Siepel & Van de Bund (1988).

- 100 >

u ID 80 +>^- OI. +-• IA !E

20-

o a o

3456789 10 11 Depth in meters below maximum level of barrage

Figure 3.4. Proportion of mites with life-history tactic VIII (facultative diapause or quiescence) plotted against the depth in meters beneath a com­ pletely filled storage reservoir in Germany. Data from Tamme tal . (1984).

58 Applications of tactics

Bothfertilizatio nan dcattle-grazin gle dt oa microarthropo dcommunit y moreadapte d todisturbance .Th e speciesoccurrin gar eabl e tofle e either inspac e (phoretics)o ri ntim e (diapause).Predictabilit y ofth eenviron ­ ment decreased which canb e concluded from the lower fractiono fthelyto - kously reproducing species compared to sexually reproducing species.

The microarthropod community of an annually drained flood plain

Data on themite s of anannuall y drained flood plainar e provided by Tamm et al. (1984). Thedominan tactinedi dspecie sNeomolgu sobsoLetu s(Berlese )an dCheylostigmaeu spannonicu sWillman n have thepossibilit y of long submergence inth e egg stage (Tamm 1984): tactic VIII. In Figure 3.4 the proportion of life-history tactic VIII (facultative diapause orquiescence ) isplotte d againstth edept h inth estorag ereser ­ voir beneath maximal water level (completely filled reservoir). The more under themaximu m level,th emor eunpredictabl e theenvironmen tbecome s in terms of chance of submergence. The increase of the proportion of life- history tacticVII Iwit h increasingdept h issignifican t (F-test: p<0.05). Consistentwit h thefift hhypothesi s anincreas e ofth efractio no fmicro - arthropods having facultative diapause or quiescense (tactic VIII) with increased chance of submergence was found. This clearly illustrates the unpredictability in time of such abiotope .

The effect of persistent pollutants

Pollution with heavy metals and persistent pesticides may substantially alter themicroarthropo d community inth e long run.Th e following studies withdat ao nmicroarthropods , (almost)al lidentifie dt oth especie slevel , allow evaluation of pollution effects over a long period of time.

Heavy metal pollution

Data on species composition of Collembola in a transect up to 20k m away from a brass mill were presented by Bengtsson and Rundgren (1988). Presumably because of their different soil types, three of their eight sample sites (XI, IV and VI) had a significantly lower pH(H20) (F-test: p-0.025), a lower CEC (F-test: p<0.001), and a lower Ca content (F-test: p<0.001)a s calculated from their table 1.Thes e siteswer e excluded from the present analysis. The dominant species were: Willemia aspinata Stach 1949,W . anophthalmia Borner 1901,Onychiuru s absoloni (Borner 1901), 0. armatus (Tullberg 1869), Tullbernia callipygosBorne r 1902,T . sylvatica Rusek 1978,T .tenuisensillat a (Rusek 1978), T. italica/vossi. T.macrochaet a (Rusek 1978), Folsomia fimetarioides (Axelson 1905),F .Candid a (Willem 1902), Isotomiellamino r (Schaffer 1876)an d Isotoma notabilis (Schaffer 1896), allo f themhavin g athelytokou s reproduction and arelativel y shortlife ­ time:tacti cX (Petersen 1971,1980 ;Gregoire-Wib o &Snide r 1984;Va nStraale n et al. 1985). Dominant specieshavin gsexua lreproductio n (tacticXI )were :Friese amirabili s (Tullberg 1871),Anurid apygmae a

59 Microarthropodcommunitie s

(Borner 1901), Folsomiaguadrioculat a andLepidocyrtu s lanuninosus (Gmelin 1788)(Gregoire-Wib o1974 ; Hale 1965). Figure3. 5present sth epercentag eo foccurrenc eo fthelytokousl yrepro ­ ducingcollembolan s(tacti cX )a tth efiv eremainin gsite si nth etransec t fromth ebras smill .Th edecreas ei ntacti cX wit hincreasin gdistanc efro m thebras smil lwa ssignifican t (F-test:p<0.05) . Themos tpollute dsite s mainlyha dCollembol awit ha thelytokou sreproduction .

X10 0 u '•uM «J +•»

L. O s: 90

jo o A e .£ 80H o U

o a o 70 1000 2000 3000 4000 5000 6000 7000 8000 Distancei nmeter sfro m brassmil l

Figure 3.5. Proportion of Collembola with life-history tactic X (thely­ tokous reproduction and relatively short lifetime) plotted against the distance (in meters) from a brass mill in Gusum (Sweden) . Data from Bengtsson & Rundgren (1988).

60 Applicationso ftactic s

Table3.2 .Percentage so findividual spe rlife-histor ytacti co fth e microarthropodsi na fores tsoil :A=contro lplot ,C=5 0k gH S O ha and D=150k gH S O ha" appliedannually .Base do nBâât he tal .(1382) . "-"" "* "2"~4' " Life-historytacti c A C D

II 0.03 0.25 0.04 III 6.85 5.99 6.30 V 0.14 0.09 0.15 IX 0.99 0.83 2.58 X 24.99 37.61 47.13 XI 66.77 54.79 43.69 XII 0.22 0.43 0.11

! UNTREATED FIELDS 2

DDT1 DDT 2 DDT 3

Figure 3.6. Life-history tactics of microarthropods (mites and spring- tails), sampled in 1986, in a long-term DDT application experiment in Wageningen (The Netherlands). Two plots received no DDT (untreated); DDT1 received 300 mg.m~2y~\ DDT2 600 mg.m~2yr, and DDT3 2000 mg.m~zyr~l from 1953-1968. Data from Van de Bund (unpublished).

61 Microarthropod communities

Experimental acidification

The data ofBâât h et al. (1982)concer nbot h Collembola andAcar i sampled in 1976 after sixyear s of artificial application of acid rain. The dominant species at their sites are: "Brachychthoniidae", sexual reproduction is assumed here foral lmember s of the family although confirmed foronl y one (West 1982): tactic XI; the same tactic is given for Nanorchestes arboriger (Berlese). Tectocepheus velatus. Oppiella nova and Tullbernia krausbaueri have thelytokous reproduction (tactic X) and Schwiebea spec, are facultative phoretics (tacticII) . Table3. 2 liststh epercentage so fth elife-histor y tacticspresent .Th e observed increase inthelytokousl y reproducingmicroarthropod s (tactic X) was almost significant p=0.06 (F-test). Hence, artificial acidification seemst olea dt oa nincreas ei nth eproportio no fthelytokousl y reproducing species already after sixyears .

Persistent pesticides

Long-term effectso fDD Thav ebee n studiedb yVa nd eBun d (1965,1976) . In 1986h esample d themicroarthropo d faunao f thesam eplot sagai nan d found the remnants of DDT and dérivâtes about 30%o f the total amount supplied (Vand eBund ,unpublished ,Martij n et al. 1993). Figure 3.6 presentslife - history tacticso fmicroarthropod s intw ountreate dplot s (noDD T applied) and three treated plots in1986 . Dominant species in the plots were: Tullbergia krausbaueri. Isotoma notabilis. Microppia minus. Oppiella nova and Tectocepheus velatus. all thelytokously reproducing species (tactic X), and Cosmolaelaps claviger (Berlese 1883)an dArctoseiu s cetratus (Sellnick 1940)phoreti c asadult s (Afifi 4 Van derGees t 1984; Binns 1974): tactic IV. The obvious increase of the proportion of thelytokously reproducing microarthropods issignifican t (F-test p<0.05). The additiono fa persis ­ tent pesticide to the soil apparently made the environment more suitable forthelytokousl yreproducin g thanfo rsexuall yreproducin g species,whic h is consistent with hypothesis 6.

DISCUSSION

Bothi nheav ymeta lpollute dan di npersisten tpesticid epollute darea sth e proportiono fthelytokousl yreproducin gmicroarthropod sincreased .I nChap ­ ter2 i twa spointe dou ttha tthelytok y isfavoure di nconstan trathe rtha n invariabl ebiotopes .I tseem stha tth epresenc eo fa ver ydominatin genvi ­ ronmental factor, which is constantly present, has the same effect. The clone(s)o f the thelytokous species,presen t at those sites and resistant toth epollutant ,o rabl e toavoi d it,ma yreproduc emor e effectively than otherclone san d thansexuall y reproducing species.I nth esexuall yrepro -

62 Applicationso ftactic s ducingspecie sa nwell-adapte dgenotyp ema yb edisrupte dever ytim ei nre ­ production.Th eproportio no fthelytokousl yreproducin gmicroarthropod st o theirtota lnumbe rma yb ea goo dindicato ro fpersisten tpollutants ,appa ­ rentlyo fan ykind . Sucha thelytokousl y reproducingpopulatio no fmicroarthropod scanno t be considered 'adapted' toth echange d environment.Par t ofth einitia l population (oneo ra fe wclones )ma yb ychanc eb eresistan tt oth epollu ­ tant or able to avoid it. So, the genetic variability in the initial (beforepollution )population ,o ri nreferenc epopulation s inunpollute d areasi sexpecte dt ob emuc hhighe rtha ni nth epopulatio ni nth epollute d environment.Suc ha neffec ti si ncontras twit hth eeffec to fintermediat e (ir)regulardisturbance swhic hresul ti na hig hclona ldiversit yaccordin g toSeben san dThorn e (1985). Thecommo nus eo fthelytokou sspecie si nlaborator yexperiment st oeva ­ luateth etoxicit yo fpollutant san dt oextrapolat eth eoutcom et ospecie s assemblagesi sope nt ocriticism .Ironically ,man ylaborator yexperiment s onthi ssubjec tar ecarrie dou twit hthelytokousl yreproducin gspecies :i n microarthropods e.g. Folsomia Candida by Butcher and Snider (1975)an d Thirumurthi and Lebrun (1977); Onychiurus armatus by Bengtsson et al. (1983a, 1985a, 1985b), Platynothrus peltifer by Streit (1984) and Van Straalen et al. (1989);an di nearthworm se.g . Eisenia foetida (partheno- geneticaccordin gt oGavrilo v1960 ,bu tse eVa nGeste l1991 )b yHartenstei n et al. (1981); Dendrobaena rubida (partly parthenogenetic according to Evans andGuild ,1948 )b yBengtsso n et al. (1983b,1986 )an d Octolasium cyaneumb yStrei tan dJaegg y(1983 )an dStrei t(1984) .Thelytokou sspecies , especially when sampled froma pollute d environment,ca nb eexpecte dt o yieldbiase dtoxicit ytes tresults ,a ris kwhic hwoul db eles si nsexuall y reproducing species. The list of conditions for a representative soil organism to study ecotoxicological effects given by Bengtsson et al. (1983b) has to be extended with: 'the species must have sexual reproduction'. Fromth eresult spresente di nthi spape ri tshoul db eobviou sthat ,ba ­ sedo nth elife-histor ytactic so fspecie si ti spossibl et omak ecompari ­ sonso fth eimpac to fmanagemen tmeasure s indifferen tbiotope s(forest , grassland,annuall ydraine dfloo dplains )an dth eeffec to fpollutio n(DDT , heavymetals ,acidification )i ndifferen tarea s(Germany ,Th eNetherlands , Sweden)o nth esoi lmicroarthropo dcommunity .So ,i tseem slikel ytha tth e systemo flife-histor ytactic sca nb eapplie di nvariou sarea so fpractica l importance.

63 Microarthropod communities

REFERENCES

Afifi, A.M. & L.P.S. van der Geest, 1984. Notes on the development and biology of the predaceous soil mite Cosmolaelaps claviger (Berlese, 1883) (Gamasida: Laelapidae). In :Acarolog y VI, Vol 1,585-590 . Athias-Binche, F., 1981. Ecologie des uropodides édaphiques (Arachnides: Parasitiformes) de trois écosystèmes forestiers. 1. Introduction, matériel,biologie . Vie Milieu 31,137-147 . Athias-Binche, F., 1984.L a phoresie chez les acariens uropodides (Anactinotriches), une stratégie écologique originale. Acta Oecologia/Oecologia Generalis 5,119-133 . Bààth, E., B . Berg,U . Lohnt,B . Lundgren,H . Lundkvist, T. Rosswall, B. Soderstroem & A. Wiren, 1980. Effects of experimental acicificationan dlimin go nsoi lorganism s anddecompositio n ina Scot s pine forest. Pedobiologia 20,85-100 . Bengtsson, G., T. Gunnarsson & S. Rundgren, 1983a. Growth changes caused by metal uptake in a population of Onychiurus armatus (Tullb.) (Collembola)feedin g on ameta l polluted fungus. Oikos 40,216-225 . Bengtsson, G., S. Nordstrom & S. Rundgren, 1983b. Population density and tissue metal concentration of lumbricids in forest soils near abras s mill. Environmental Pollution SeriesA 30,87-108 . Bengtsson, G., T. Gunnarsson & S. Rundgren, 1985a. Influence of metals onreproduction ,mortalit y andpopulatio n growth inOnychiuru s armatus (Collembola). Journal of Applied Ecology 22,967-978 . Bengtsson, G., L. Ohlsson & S. Rundgren, 1985b. Influence of fungi on growth and survival of Onychiurus armatus (Collembola) in a metal polluted soil. Oecologia 68, 63-68. Bengtsson, G., T. Gunnarsson & S. Rundgren, 1986. Effects of metal pollution on the earthworm Dendrobaena rubida (Sav.) in acidified soils. Water Air Soil Pollution 28,361-383 . Bengtsson, G. & S. Rundgren, 1988. The Gusum case: a brass mill and the distribution of soilCollembola . CanadianJourna l of Zoology 66,1518 - 1526. Binns, E.S., 1974. Notes on the biology of Arctoseius cetratus (Sellnick) (Mesostigmata: Ascidae). Acarologia 16,577-582 . Binns, E.S., 1982. Phoresy as migration - some functional aspects of phoresy inmites . Biological Reviews 57,571-620 . Bund, CF. van de, 1965. Changes in the soil fauna caused by the application of insecticides. Bolletino di Zoologica Agrarica e Bachicoltura Series II. 7, 83-112. Bund, C.F. van de, 1976. Side effects on the soil fauna in arable land by insecticides. Bulletin SROP/WPRS Bulletin 1976/3, 33-42. Bund, C.F. van de & H.J .P . Eysackers, 1986. Veldonderzoek naar de mogelijke neveneffecten van Dimilin, toegepast tegen nonvllnder, op bodemarthropoden(Luyksgeste ld eKapel ,voorjaa r 1986). Internalrepor t ResearchInstitut e forNatur eManagemen t87/3 ,Arnhem ,Th eNetherlands . Butcher, J.W. & R.M. Snider, 1975.Th e effect of DDT on the life history of Folsomia Candida (Collembola: Isotomidae). Pedobiologia 15, 53-59. Desender, K. & M. Vaneechoutte, 1984. Phoretic associations of carabid

64 Applications of tactics

beetles (Coleoptera,Carabidae )an dmite s (Acari). Revue d'Ecologie et Biologie du Sol 21, 363-371. Evans,A.C . & W.J.Mc.L. Guild, 1948. Studies on the relationship between earthworms and soil fertility. IV. On the life cycles of some British Lumbricidae. Annals ofApplie d Biology 35,471-484 . Gavrilov, K., 1960 . La sexualidad y la reproducion de los Oligochaetos. Acta Trab. 1. Congress Sudan Zool. 2,145-155 . Glesener, R.R. & D. Tilman, 1978. Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals.America n Naturalist 112,659-673 . Grandjean, F., 1941. Statistique sexuelle et parthénogenèse chez les Oribates (Acariens). Compte rendu hebdomadaire Seance Academie Scientifique Paris, 212,463-467 . Grégoire-Wibo, C, 1974.Bioecologi e de Folsomia quadrioculata (Insecta, Collembola). Pedobiologia 14,199-207 . Grégoire-Wibo, C. & R.M. Snider, 1983.Temperature-relate d mechanisms of population persistence in Folsomia Candida and Protaphorura armata (Insecta, Collembola).Pedobiologi a 25,413-418 . Grime, J.P., 1977. Evidence for the existence of three primary strategies inplant s and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169-1194. Grime, J.P., 1979. Plant strategies andvegetatio n processes.Joh n Wiley & Sons, New York. Grime,J.P., J.G . Hodgson & R. Hunt, 1988.Comparativ e plant ecology. A functional approach to common British species.Unwi n Hyman, London. Hale, W.G., 1964. Experimental studies on the taxonomie status of some members of the Onychiurus armatus species group. Revue d'Ecologie et Biologie du Soll,501-510 . Hale, W.G., 1965.Observation s on thebreedin g biology of Collembola. Pedobiologia 5, 146-152,161-177 . Hartenstein, R., E.F. Neuhauser & A. Narahara, 1981. Effects of metal and other elemental additives toactivate d sludge ongrowt h of Eisenia foetida. Journal of Environmental Quality 9, 23-26. Holm, E., 1988. Environmental restraints and life strategies: a habitat templet matrix. Oecologia 75,141-145 . Karg, W., 1971.Acar i (Acarina), MilbenUnterordnun g Anactinochaeta (Parasitiformes), Die freilebenden Gamasina (Gamasides), Raubmilben. Die Tierwelt Deutschlands 59,Gusta v Fischer Verlag,Jena . Karg, W., 1987. Zur Kenntnis der Gattung Schwiebea Oudemans, 1916 (Acarina,Sarcoptiformes) . Deutsches entomologisches Zeitschrift,Neu e Folge 34,141-148 . Krczal, H., 1959. Systematiek und Oekologie der Pyemotiden. Beiträge zur Systematik und Oekologie mitteleuropäischer Acarina 1, Abschnitt 3, 385-625. Lindquist, E.E., 1986. The world genera of Tarsonemidae (Acari: Hetero­ stigmata):a morphological ,phylogenetic ,an dsystemati crevision ,wit h a reclassification offamily-grou p taxa inth eHeterostigmata . Memoirs of the Entomological Society of Canada 136, 1-517. Luxton, M., 1966. Laboratory studies on the feeding habits of saltmarsh acarina,wit h notes on theirbehaviour .Acarologi a 8, 163-175. Luxton,M .,1967 .Th ezonatio no fsaltmars hAcarina .Pedobiologi a7 ,55-66 .

65 Microarthropod communities

Luxton, M., 1981. Studies on the oribatid mites of a Danish beech wood soil. IV. Developmental biology. Pedobiologia 21,312-340 . Martijn, A., H. Bakker & R.H. Schreuder, 1993. Soil persistence of DDT, Dieldrin, and Lindane over a long period. Bulletin of Environmental Contamination and Toxicology 51,178-184 . McArthur, R.H. & E.O. Wilson, 1967.Th e theory of island biogeography. PrincetonUniversit y Press,Princeton , N.J. Petersen, H., 1971. Parthenogenesis in two species of Collembola: Tullbergia krausbaueri (Boerner) and Isotoma notabilis (Schaeffer). Revue d'Ecologie et Biologie du Sol 8,133-138 . Petersen,H. , 1980.Populatio n dynamic and metabolic characterization of Collembola species in a beech forest ecosystem. In: Dindal, D.L. (ed.) Soil biology as related to land use practises. ProceedingsVII . International Soil Zoology Colloquium ofth e I.S.S.S., Syracuse,N.Y ., 806-833. Sebens, K.P. & B.L. Thorne, 1985. Coexistence of clones, clonal diversity, and disturbance. In:Jackson ,J.B.C. ,L.W . Buss& R.E . Cook (eds). Population biology and evolution of clonal organisms. Yale University Press,Ne w Haven & London,357-398 . Sengbush, H.G., 1958. Zuchtversucherait Oribatiden . Naturwissenschaften 45, 498-499. Siepel, H., 1990.Decompositio n of leaves ofAvenell a flexuosa and microarthropod succession in grazed and ungrazed grasslands. I. Succession ofmicroarthropods . Pedobiologia 34, 19-30. Siepel, H. & C.F. van de Bund, 1988. The influence of management practices on the microarthropod community of grassland. Pedobiologia 31, 339-354. Southwood, T.R.E., 1977.Habitat , the templet for ecological strategies? Journal ofAnima l Ecology 46,337-365 . Southwood, T.R.E., 1988.Tactics , strategies and templets.Oiko s52 , 3-18. Stearns, S.C., 1976. Life-history tactics: a review of the ideas. Quarterly Review of Biology 51,3-47 . Straalen, N.M. van, H.A. Verhoef & E.N.G. Joosse, 1985. Functionele classificatie van bodemdieren en de ecologische functie van de bodem. Vakblad voor Biologen 65,131-135 . Straalen, N.M. van, J.H.M. Schobben & R.G.M, de Goede, 1989. Population consequenceso fcadmiu mtoxicit y insoi lmicroarthropods . Ecotoxicology and Environmental Safety 17,190-204 . Streit, B., 1984. Effects of high copper concentrations on soil invertebrates (Earthwormsan doribati dmites) : Experimentalresult san d a model. Oecologia 64,381-388 . Streit, B., & A. Jaeggy, 1983. Effect of soil type on copper toxicity and copper uptake inOctolasiu m cyaneum (Lumbricidae). In: LebrunPh . et al. (eds)Ne w trends in soilbiology : 569-575. Taberly, G., 1987. Recherches sur la parthénogenèse thélytoque de deux espèces d'acariens oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). I.Acarologi a 28,187-198 . Tamm, J.C., 1984. Surviving long submergence in the egg stage - a successful strategy of terrestrial arthropods living on flood plains (Collembola, Acari, Diptera). Oecologia 61,417-419 .

66 Applications of tactics

Tamm, J.C., H.-W. Mittmann & S. Woas, 1984. Zur Landmilbenfauna eines Jahres-periodischtrockenfallende nStauseebodens .Pedobiologi a27 ,395 - 404. Thirumurthi, S. & Ph. Lebrun, 1977. Persistence and bioactivity of Carbofuran in a grassland. Mededelingen der Faculteit Landbouwwetenschappen Rijksuniversiteit Gent42/2 . Van Gestel, C.A.M., 1991. Earthworms and ecotoxicology. Thesis. University ofUtrecht , The Netherlands. West, CC, 1982. Life histories of three species of subantarctic oribatid mite. Pedobiologia 23, 59-67. Woodring, J.P. & E.F. Cook, 1962. The biology of Ceratozetes cisalpinus Berlese, Scheloribates laevigatusKoch ,an dOppi aneerlandic a Oudemans (Oribatei), with a description of all stages.Acarologi a 4, 101-136.

67 Microarthropod communities

Appendix 3.1. Key to the life-history tactics of microarthropods.

1 - the species isphoretic , either obligately or facultatively, not just accidentally 2 - the species isno t phoretic or just accidentally phoretic 6 2 -th e species feeds on thehost/carrie r as an important food source in one or all life stages attached to the host/carrier 3 - the species does not feed on the carrier, or the carrier can at least not be considered an important food source inan y life stage attached to the carrier 4 3 -th e species is free-livingpar t of its life cycle Tactic lb - the species spends its entire life cycle on thehos t Tactic la 4 -th e species iseithe r facultatively phoretic, or obligately phoretic but in the latter case with a comparatively low development rate, or a low egg production; all types of reproduction possible Tactic II - the species isobligatel y phoretic,ha s a fast development rate and relatively high eggproduction ; sexual or arrhenotokous reproduction only 5 5 -juvenil e stages of the species are phoretic only, often specially adapted forphoreti c transport Tactic III - the species isphoreti c inan y stage including adults Tactic IV 6 -th e speciesha s an obligate or facultative diapause in its life cycle, or synchronization of its life cycle by quiescence during some period(s) 7 - the speciesha s continuous generations inwhic h development can be slow in some periods,whic h isno t considered a quiescence 10 7 -th e species has anobligat e diapause or obligate aestivation, or alternate generations have one of these Tactic V - the speciesha s a facultative diapause or quiescence 8 8 -th e species has ananemochorou s dispersal Tactic VII - the dispersal of the species isno t predominantly anemochorous 9 9 -th e species has a semelparous oviposition Tactic VI - the species has an iteroparous oviposition Tactic VIII 10 -th e species has a thelytokous reproduction 11 - the speciesha s a sexual reproduction 12 11 -th e species is relatively short living Tactic X - the species is relatively long living Tactic IX 12 -th e species has an iteroparous oviposition Tactic XI - the species has a seasonal iteroparous oviposition Tactic XII

68 Feeding guilds of oribatid mites

based on their carbohydrase activities

SUMMARY. Carbohydraseactivit ywa sanalyse di n4 9specie so foribati dmite s andon eacaridi dmit esample dfro mnatura lpopulations .Enzym eactivit ywa s determined for the main differentiating food components: cellulose, a component of cell-walls of green plants; chitin, a component of fungal cell-walls; and trehalose, a component of fungal cell-contents. Feeding guildswer e defined based onth e activity of the three carbohydrases. The nomenclature ofth efeedin gguild swa sadopte dfro mtha to fruminants .Fiv e major feeding guildswer edistinguished :herbivorou s grazers (9 species), fungivorous grazers (8), herbo-fungivorous grazers (16), fungivorous browsers (7)an d opportunistic herbo-fungivores (8)an d twomino r guilds in oribatids: herbivorous browsers (1) and omnivores (1).Th e feeding guilds presented are operationally better defined in terms of resource exploitation than the macro-,micro - and panphytophages used hitherto.

INTRODUCTION

Feeding guilds of phytophagous oribatid mites have been defined by Schuster (1956), and refined by Luxton (1972) and various authors since (e.g. Kaneko, 1988;Wallwork , 1983). The classification of feeding types in guilds is important to understand the role a species plays in its biotope. Their function in the decomposer community might be comminution of organic matter, alteration of microbial activity or dispersal of decomposer micro-organisms (Wallwork, 1983; Swift et al., 1979; Behan and Hill, 1978), and some species may be ground-dwelling herbivores without any function in decomposition. The current classification into three phytophagous guilds i.e. macrophytophages (feeding onhighe r plant

69 Microarthropod communities material, either wood or leaf), microphytophages (feeding strictly on the microflora) and panphytophages (feeding on all kinds of plant or fungal tissues) is based primarily on the function oribatid mites were thought to have: fragmentation of litter. It has become clear that ori- batids may also have an influence on decomposition through grazing on fungi and bacteria (Van der Drift and Jansen, 1977;Hanlon , 1981; Hanlon and Anderson, 1979). The present descriptions of feeding guilds are not specific enough with respect to this influence on decomposition. Micro- phytophages for instance may feed on bacteria or fungi (and influence decomposition), or on algae (without decomposer function), or any combination of those (Luxton, 1972); so it is not easy to relate this guild to any specific decomposer function. For a reliable relationship between the possible function of species in the decomposer community and the feeding guild the latter must be defined as strictly and uniquely as possible. Hofmann and Stewart (1972) classified East African ruminants into two major groups: roughage eaters or grazers having a subdivided, capacious rumen with uneven papillation; and concentrate selectors or browsers having a relatively small rumen adapted to a fast turnover of food. Between these two groups an inter­ mediate group was distinguished. Our nomenclature of feeding guilds of oribatid mites is similar to this classification in the use of the terms: grazer and browser. Grazers have the ability to digest both cell- walls and cell-contents;browser s are only able to digest cell-contents. In our study feeding guilds are based on the capabilities of oribatid mites to digest plant or fungal tissues, i.e. cellulose, a major com­ ponent of green plant cell-walls; chitin, a major component of fungal cell-walls; and trehalose, a component of fungal cell-contents (the combination of both chitin and trehalose is probably unique for fungi, Hegnauer, 1962). Trehalose is also found in lichens (Darnley Gibbs, 1974), in Cyanophytae, to some extent in Rhodophyta and in Selaginel- laceae (Hegnauer, 1962), and in Myxophyta (Hegnauer, 1986). In excep­ tional cases it has been found in reasonable amounts in higher plants (Hegnauer, 1963). Darnley Gibbs (1974) reported it from higher plants under environmental stress, especially drought. In our study the diges­ tive capabilities of mites were measured by their cellulase, chitinase and trehalase activity in field populations.

It was not our aim to define exactly which compounds a mite can digest. The three enzymes mentioned were selected to yield the best differentiation in terms of feeding guilds. Carbohydrase activity on a qualitative basis has been studied before in oribatid mites by Luxton (1972, 1979) and Zinkler (1970)wh o made also some quantitative measure­ ments. Maybe other groups of gut enzymes, e.g. esterases and proteases in future can also be used to differentiate between feeding patterns if

70 Feedingguild s

theseenzyme sac to nfoodtyp especifi ccomponents .I nou rstud yactivit y measurementso fth ethre ecarbohydrase swer ecarrie dou tquantitatively .

MATERIALSAN DMETHOD S

Analyseso fcarbohydras eactivit ywer ecarrie dou ti nmite ssample dfro m naturalpopulations ,t opreven tdrawin gconclusion so nenzym eactivitie s whichmigh tb einduce di npopulation sreare d inth elaboratory .Fro mMa y until November 1989 living mites were sampled from various biotopes: soil, litter, moss (both on trees and on solid surfaces), lichens, herbage,tree san dsphagnu mpools .Fo ranalysi so fth eactivit yo fthre e carbohydrases (cellulase,chitinas ean dtrehalase )4 9o fth emos tcommo n species of oribatid mites and one species of acaridid mite were selected; the oribatid mite species chosen were selected as far as possible from the different families according to Balogh (1972) and Marshall etal . (1987).Th eacaridi dmit ewa sadde d toth e listbecaus e itwa s thought torepresen t afeedin g guild (abrowser )whic hmigh tb e notcommo namon goribatids . To identify the specieswhe n alive arathe r laborious methodha dt o be followed. Species were extracted from substrate and prepared for microscopic inspection as described by Siepel and Van de Bund (1988). Whenon eo fth eoribati dmit e specieswa snumerou s inth esubstrat ean d no confusion could arise with any other species, that substrate was sampled for living mites of that species. If no species in that substratecoul db esample daliv ewithou tconfusio nwit hothe rspecies ,a substrate was sampled elsewhere and the procedure started again. Iti s because of this procedure that no members of Brachychthoniidae and Suctobelbidae andonl yon emembe ro fOppiida e (Ramusella clavipectinata) were included in this study. In these families many species were regularly present together which impeded a reliable identification of the mites to be analysed. Four replicate samples were obtained at differentsamplin gdate san ddifferen tlocalities . Thesubstrate s soil,litter ,moss ,lichens ,an dsphagnu mwer esample d andplace d ina Tullgre n funnel tocollec t themite s inwater .Herbag e and trees were sampled using a sweep net; these samples were put in water and the mites were removed by hand sorting. The live miteswer e counted and about 250/i gmit e freshmas swa spu t inon e glass tubepe r enzyme analysis. The number of mites per analysis varied from 1 (also whenth emit eweighe dmor etha n25 0/ig )u p to9 0specimens .I nth eana ­ lyses ofcarbohydras e activity in Licneremaeus licnophorus 80specimen s

71 Microarthropod communities were used which corresponded to about 100 /ig.Th e mites were pulverized just before the incubation. Activity of cellulase (ß 1-4 glucan-glucano-hydrolase, EC 3.2.1.4) was determined by colorimetrically measuring the amount of glucose at 444 nm after colouring with Sigma method no 510 (1 capsule in 50 ml water and 1.6 ml colour reagents) during 45 min at room temperature. Glucose is the product of animal cellulase activity after 4 h in a IX carboxymethylcellulose Sigma C-8758 at pH - 5.0 (created by addition of phosphoric acid) and 37°C (Siepel, 1990). Activity of chitinase (poly /8-l,4-(2-acetamido-2-deoxy )-D-glucosid e glycano hydrolase, EC 3.2.1.14) was determined by colorimetrically measuring the amount of acetyl-glucosamine at 585 nm after boiling for

10 min, dissolving 100m l 0.8 M K2B407 in 0.5 ml reagents, again boiling for 3 min, and adding 1 g p-dimethyl benzaldehyde in 100 ml 98% acetic acid with 1.2% 12N HCL (Jeuniaux, 1966). Acetyl-glucosamine is the product of animal chitinase activity after 4 h in a 0.5% suspension of chitin (Sigma C-3641) at pH - 5.1 (created by 0.6Mcitri c acid and1.2 M bisodium hydrogen phosphate) and 37°C (Siepel, 1990). Activity of trehalase (a,a'-glucosid e 1-glucohydrolase, EC 3.2.1.28) is determined by measuring the amount of glucose as described above under cellulase activity assay. Glucose is the product of animal treha­ lase activity after 4 h in a 1% trehalose solution (ct,D-glucopyranosyl- a,D-glucopyranoside) Sigma T-5251 at pH 5.7 (created by addition of phosphoric acid)an d 37°C (Siepel, 1990). For every carbohydrase activity measurement (cellulose, chitinase or trehalase) four replicate samples were analysed. In addition to the samples for analysis of carbohydrase activity blanks samples were also prepared. The procedure for these blanks was the same except for the omission of the incubation period at37°C .

RESULTS

In Table 4.1 carbohydrase activities are presented for the mite species investigated, ranked per feeding guild. When a blank result did not differ significantly from the mean of the incubated samples, it was concluded that the activity of the enzyme was negligible; this concerned lowvalue s only. Based on the carbohydrase activities the oribatid mites were classi­ fied into five major guilds and two small ones with one species each as mentioned inTabl e 4.1. The feeding guildswil l now pass in review.

72 Feedingguild s

Herbivorous grazers:hav e cellulase activityonly ,fee d ongree nplant s (includingalgae )an dar eabl et ofee do nbot hth ecell-content san dth e cell-walls.Th enin e species inthi sguil d canfee do nlivin gplant sa s well as on litter and are intha t case important as comminutors inth e decomposer community. A comparatively low cellulase activity suggests either a low metabolic rate or a transition towards the next feeding guild. Herbivorous browsers: defined by the absence of activity of the three enzymes analysed. This may well apply for most predators, carrion feeders and bacteria feeders, too. Feeding experiments must differen­ tiatehere .Th eonl y species inthi s "guild" is Melanozetes mollicomus, which might be a carrion feeder just like the related Fuscozetes fuscipes (Wallwork,1958) . Funpivorous grazers: have chitinase activity as well as trehalase activity.Th eeigh tspecie si nthi sguil dfee do nfungi ,an dar eabl et o digestbot hcell-wall san dcontents .O fcours ethes especies ,becaus eo f their chitinase activity canals o feed ondea d mycelium, something the nextguil d isunabl e to.Specie swit hrelativel y lowchitinas eactivit y (compared with other species andwit h their trehalase activity)ma yb e transitional cases to the next guild. Species having both lower chitinasean dtrehalas eactivit yma yb emetabolicall y lessactive . Funpivorousbrowser s: ar e able to digest trehalose only. The onlyaca - ridid mite investigated belongs to this guild, as expected. Unexpected was the presence of a rather large number of oribatids. The lower trehalase activities of some species probably do not indicate lower metabolic rates,whic h seemsrathe runlikel yher ebecaus e ofth eactiv e mode ofbehaviou r of these species.A transition,however , towards the group ofherbivorou s browsers isquit e probable,especiall y when iti s noted that these species might be lichenovorous browsers, because trehalose also occurs in lichens (Darnley Gibbs, 1974). The licheno­ vorousbrowse rmigh tb e defined ashavin g acomparativel y lowtrehalas e activity,becaus ea substantia lpar to fit sdie ti so falga lorigin . Herbo-funpivorous prazers: are able to digest allmai n food components ofbot hgree nplant san d fungi.Thi s isth ebigges tguil d foundwit h1 6 specieso fwhic h fivear egenuin eherbo-fungivores ,becaus e theyhav ea relatively high enzyme activity of all three enzymes: Nothrus silvestris, Nanhermannia elegantula, Phauloppia lucorum, Humerobates rostrolamellatus and Acrogalunma longipluma. Lichenovory is also pos­ siblehere ,whic hprobabl yhold s forP . lucoruman d H. rostrolamellatus (Seydan dSeaward , 1984).On especie sma yb e atransitiona l caset oth e fungivorous grazers: Chamobates schütz!, and one species to the next guild: Trichoribates trimaculatus. The other species here show a relationship toth eguil do fth eherbivorou sgrazers .

73 Microarthropod communities

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74 Feeding guilds

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75 Microarthropodcommunitie s

Opportunistic herbo-funpivores: are able to digest cellulose inlitte r andcell-wall so flivin ggree nplant san dtrehalos e infungi .Thei rmai n food itemprobabl y consists ofgree nplants .The y can takeadvantag eo f periodic increases in fungal growth in their biotopes: a rather opportunistic feeding strategy. As has been pointed out already under the heading of the fungivorous browsers, ability to digest trehalose might also point to lichenovory. Especially the species from dry biotopes mightb e classified into the lichenovorous grazers.Th e guild ofopportunisti c herbo-fungivores canb edivide d intw ogroup sbase do n the biotope they live in; a (semi)aquatic group (Trhypochthoniellus excavatus, Hydrozetes lacustris, Liwnozetes foveolatus) whichmigh tals o feed additionally on Cyanophyta (containing both cellulose and treha­ lose),an da secon dgrou plivin gi ntemporarily-favourabl emicrobiotope s (mosso ntree so rstones ,droppe dcone so falder ,etc. )(Wallwork ,1983 ) comprising Camisia spinifer, Adoristes ovatus, Carabodes labyrinthicus, Tectocepheus velatus, and Scutovertex minutus, whichma y feedo nlichen s (alsocontainin gbot hcellulos ean dtrehalose) . Omnivores: an unexpected guild to be distinguished on the basis of carbohydrases.However ,th epresenc eo fcellulas eactivit yclearl yindi ­ catesherbivor yan dth epresenc eo fchitinas eactivit ywithou ttrehalas e activity is quite peculiar for fungal feeding only (able todiges tth e cell-wall, but not one of the major components of the cell-contents). Soil dwelling organisms having chitin and lacking trehalose ascompo ­ nents are arthropods only. It isconcluded , that species of thisguil d feedo nplant s and a chitin containing food source: arthropods .Hence , theyar eomnivores .On especie swa sfound : Hypochthonius rufulus.

DISCUSSION

Therol eo fth egu tmicroflor a

One of the first questions arising in determination of carbohydrase activities iswhethe rthes eenzyme sar eo fanima lo rmicroflora lorigin . Someauthor shav e showntha tsom emites ,suc ha s Achipteria coleoptrata (Stefaniakan dSeniczak ,1976 )an d Oppia nitens (Seniczakan dStefaniak , 1978),hav ea workin gmicroflor ai nth ealimentar y canal,abl et odiges t morecomplicate dpolysaccharides .Fro ma necologica lpoin to fvie wi ti s not very important whether it is the enzymes of gut bacteria that breakdown foodcomponent s or theenzyme so f theanima l itself,provide d that themicroflor a active inth e alimentary canal is symbiotic inth e

76 Feedingguild s

whole population ofmites .Th e latter assumption canb ehel d regarding thelo wstandar derror si nenzym eactivit ybetwee nsample so fmite sfro m differenttime san dlocations .Luxto n(1972 )use dtoluen ea sa bacterio ­ static agent and measured little chitinase activity. As with carbohy- draseactivit yb ybacteri afro moutsid eth ebod ytoluen emigh tals ohav e stoppedth echitinas eactivit yo fth egu tmicroflor a insuc hcases .

Inductiono fcarbohydras eactivitie s

Induction of ahighe r enzyme activity may be of importance.Stefania k and Seniczak (1981) showed in Oppia nitens that the quality of food stimulated the microflora, which able to breakdown chitin. In the naturalpopulatio n chitinbreakdow n islo wa s isfoun d inthi sstud yi n the related Ramusella clavipectinata. However, when a species is not able tobrea k down chitin,enzyme s may notb e induced despite thekin d offoo d offered. In Achiptera coleoptrata for instance little chitini s broken down no matter which kind of food is offered (Stefaniak and Seniczak, 1976). The information, however, that some quantitative differences inenzym eactivit ymigh toccu rgive su sa bette ride ao fth e menuo fth efiel dpopulation ,i nwhic hseldo monl yon efoo dite mplay sa role. So carbohydrase activity gives a qualitative insight into the toolso fa species ,quantitativel y itgive sa nide ao fth erecen tus eo f such tools. The need to use all the tools (enzymes) is not always essential, and the rearing of species in the laboratory on easily- digestible food or on surplus food mayyiel d positive rearingresults , but does not give information on the field menu (Woodring, 1963). It will be no surprise when species reared in the laboratory on algae appear to digest fungi in the field. In the laboratory situationwher e food is plentiful there is no need for efficiency and probably many species will feed on the components easiest to digest (cell-contents). Walter (1987) and Walter et al. (1988) reported on carnivory among oribatids,whic h mayb e seen in this light.Th e enzymatic tools ofth e equipmento f thespecie sprov e theirvalu ewhe n foodbecome s scarcean d efficiency isneeded .A n illustrative examplema yb e theobservatio no f Woodring (1963)o f Scheloribates laevigatus feeding forsevera l dayso n fresh-cut green grass, yet this species proved to be a fungivorous grazeri nthi sstudy .

Comparisonwit hcurren tfeedin gguild s

The classification of oribatid mites in feeding guilds (Table 4.1) differs tosom eexten tfro m theclassificatio n ofLuxto n (1972)an dno t only in nomenclature. There are differences among guilds, even when

77 Microarthropodcommunitie s

Luxton's macrophytophages correspond with the herbivorous browsers and grazers together, his panphytophages correspond with both the herbo- fungivorous grazers and the opportunistic herbo-fungivores, and his microphytophages correspond with the fungal grazers and browsers here (which iscertainl y not thecas ebecaus eo fLuxton' s inclusiono falga l feedersi nth emicrophytophages) .Bot h Rhysotritia ardua and Hermaniella granulata aremacrophytophage s according toLuxto n (1972)i nhi s review table,bu tappea rt ob eabl et odiges tchiti nan dtrehalos ean dar ethu s herbo-fungivorous grazers. However, they resemble the herbivorous grazers. Kaneko (1988)foun d for R. ardua inhi s Bplo t that thegut s contained24 %hypha ean dtherefor eclassifie d ita spanphytophagous . Some of thepanphytophage s reviewed by Luxton appear tob eherbivo ­ rous grazers (thus without the capacity to digest fungal material): Achipteria coleoptrata, Parachipteria punctata, Xenillus tegeocranus and Platynothrus peltifer. Schatz (1979)foun d Achipteria coleoptrata tob e macrophytophagous. Some otherspanphytophage s reviewed by Luxtonappea r to be fungivores. Hemileius initialis is a fungivorous browser and Forsslund (1938) found mainly hyphae in its gut. The previously men­ tioned Scheloribates laevigatus is both in our study and in that of Woodring and Cook (1962) fungivorous, more precisely a fungivorous grazer. The same holds for Galumna lanceata (G. cf dorsalis inLuxto n (1972)an dVa nde rDrif t (1951),se eVa nde rHammen ,1952) ,whic hagree s withVa nde rDrif t (1951). A morepeculia r species is Tectocepheus velatus classifiedb yLuxto n (1972) as microphytophage, presented here as an opportunistic herbo- fungivore or maybe a lichenovorous grazer. This species has been a problem forman y authors:Wallwor k (1958)coul dno tobserv e anyfeedin g and foundmos tgut sempty , inhi srevie w someyear s laterh eclassifie d ita smacrophytophag e (Wallwork, 1967). Behan and Hill (1978)classif y it as microphytophage based on the gut contents of four specimens. Probably it depends on the environmental conditions what kind of food will be used by this species: a real opportunist. Trhypochthonius tectorum (Berlese 1896) classified by Luxton as a microphytophage is able to digest cellulose (cellulase activity: 132.2 ± 29.1 g glucose.mg"1 mite.4h" 1); activities of other enzymes could not be measuredbecaus e toofe wspecimen swer eavailable . Another species for which many authors give different results is Hypochthonius rufulus. Riha (1951) and Tarman (1968) found it to be necrophagous, other authors microphytophagous (Hartenstein, 1962), Farahat (1966); andWallwor k (1967)reviewe d ita sa non-specialist .I n our study it was found to be omnivorous because of its cellulase and chitinase activities.Th e species is equipped to feed on all kinds of plantan dfunga lmaterial ,bu ta hig h chitinase activity inth eabsenc e

78 Feedingguild s of trehalase activity is illogical when the species should feed substantially on fungi. In this light it is interesting to compare the reaction of the symbiotic gutflora of Oppia nitens to a carrion diet: chitinase activity is far more developed as it is in the natural population (Seniczakan d Stefaniak, 1978). The sameproces smigh toccu r inth enatura lpopulatio no f H. rufulus. Support for thisassumptio ni s found in Behan-Pelletier and Hill (1983) where in the guts of adult specimens of this speciesu p to 90%collembola n andmit e fragmentsar e recorded (means of0-352) .Whethe r H. rufulus isa scavenge r (exuviae!) ora predato r isunknown . Carbohydrase activities, especially those for the digestion of differentiating plant and fungal components, appear to give a solid basis for feeding guild definition. Quantitative data on enzyme activities permit transitions from one guild to another tob e detected andhel p tofin dth emos ttypica lrepresentativ e ofa guil dfo rfurthe r studies. It is expected that representatives of these feeding guilds will have distinctive interprétable effects on fungal activity in the decompositiono forgani cmatter .

REFERENCES

Balogh J. (1972) The oribatid genera of the world. Academia Kiado Bucharest. Behan V.M. and Hill S.B. (1978) Feeding habits and spore dispersal of Oribatid mites in the North American arctic. Revue d'Écologie et Biologied uSo l15 ,497-516 . Behan-Pelletier V.M. and Hill S.B. (1983) Feeding habits of sixteen species of Oribatei (Acari) from acid peat bog, Glenamoy, Ireland. Revued'Écologi e etBiologi ed uSo l20 ,221-267 . BlockW.C . (1965)Distributio no fsoi lmite s (Acarina)o nth eMoo rHous e National Nature Reserve Westmorland, with notes on their numerical abundance.Pedobiologi a5 ,244-251 . Darnley Gibbs R. (1974) Chemotaxonomy of Flowering Plants. Part I. McGill-QueensUniversit yPress ,Montreal ,London . DriftJ . vande ran dJanse nE . (1977)Grazin go fsprin gtail s onhypha l mats and its influence on fungal growth and respiration. Ecological Bulletin25 ,203-209 . FarahatA.Z .(1966 )Studie so nth einfluenc eo fsom efung io nCollembol a andAcari .Pedobiologi a6 ,258-268 . Forsslund K.H. (1938) Über die Ernährungsverhältnisse der Hornmilben (Oribatiden) und ihre Bedeutung für Prozesse im Waldboden. In Proceedings of the Vllth. International Congress of Entomology, Berlin, part 3, (K. Jordan and E.M. Hering, Eds) pp 1950-1957.

79 Microarthropodcommunitie s

Uschmann,W eimar . HanlonR.D.G. , (1981)Influenc eo fgrazin gb yCollerabol ao nth eactivit y of senescent fungal colonies grown on media of different nutrient concentration.Oiko s36 ,362-367 . HanlonR.D.G .an dAnderso nJ.M . (1979)Th eeffect so fCollerabol agrazin g on microbial activity in decomposing leaf litter. Oecologia 38,93 - 99. HartensteinR . (1962)Soi lOribate i I.Feedin g specificity amongfores t soil Oribatei (Acarina). Annals of the Entomological Society of America55 ,202-206 . HegnauerR . (1962)Chemotaxonomi e derPflanzen :ein eÜbersich tübe rdi e Verbreitung und diesystematisch e Bedeutung der Pflanzenstoffe.Ban d I. Thallophyten, Bryophyten, Pteridophyten, Gymnospermen. Birkhäuser Verlag,Basel . HegnauerR . (1963)Chemotaxonomi ede rPflanzen : eineÜbersich tübe rdi e Verbreitung und die systematische Bedeutung der Pflanzenstoffe.Ban d II.Monocotyledonae .Birkhäuse rVerlag ,Basel . HegnauerR . (1986)Chemotaxonomi e der Pflanzen:ein eÜbersich tübe rdi e Verbreitung und die systematische Bedeutung der Pflanzenstoffe.Ban d VII.Addendum .Birkhäuse rVerlag ,Basel . HofmannR.R . and Stewart D.R.M (1972)Graze r orbrowser ?A classifica­ tion based on the stomach structure and feeding habits of East Africanruminants .Mammali a36 ,226-240 . JeuniauxC .(1966 )[111 ]Chitinases .Method so fEnzymolog y8 ,644-650 . KanekoN . (1988)Feedin ghabit san dchelicera lsiz eo foribate dmite si n cooltemperat e forestsoil s inJapan .Revu ed'Ecologi e etBiologi ed u Sol25 ,353-363 . LuxtonM . (1972) Studies on the oribatid mites of a Danish beechwoo d soil.I .Nutritiona lbiology .Pedobiologi a12 ,434-463 . Luxton M. (1979) Food and energy processing by Oribatid mites. Revue d'Écologie etBiologi ed uSo l16 ,103-111 . Marshall V.G., Reeves R.M. and Norton R.A. (1987) Catalogue of the Oribatida of continental United States and Canada. Memoirs of the EntomologicalSociet yo fCanad a139 ,1-418 . Riha G. (1951) Zur Ökologie der Oribatiden in Kalksteinboden. ZoologischesJahrbuc hSystemati k80 ,408-450 . Schatz H. (1979)Nutritiona l biology ofOribati d mites (Acari) inhig h alpine areas of Tyrol (Obergurgl). Berichte des naturwissen­ schaftlich-medizinischenVerein s inInnsbruc k66 ,7-20 . SchusterR . (1956)De rAntei lde rOribatide na nde nZersetzungsvorgänge n im Boden. Zeitschrift für Morphologie und Ökologie der Tiere 45,1 - 33. Seniczak S. and Stefaniak 0. (1978) The microflora of the alimentary canalo fOppi aniten s (Acarina,Oribatei) .Pedobiologi a18 ,110-119 . Seyd E.L. and Seaward M.R.D. (1984)Th e association of oribatid mites withlichens .Zoologica lJourna lo fth eLinnea nSociet y80 ,369-240 . Siepel H. (1990)Nich e relationships of two panphytophagous soilmite s Nothrus silvestris Nicolet (Acari, Oribatida, Nothridae) and Platynothrus peltifer (C.L.Koch) (Acari, Oribatida, Camisiidae). Biologyan dFertilit yo fSoil s9 ,139-144 . Siepel H. and Van de Bund C.F. 1988. The influence of management

80 Feedingguild s

practices on themicroarthropo d community of grassland. Pedobiologia 31,339-354 . Stefaniak 0. and Seniczak S. (1976) The microflora of the alimentary canal of Achipteria coleoptrata (Acarl, Oribatei). Pedobiologia 16, 185-194. Stefaniak 0. and Seniczak S. (1981)Th e effect of fungal diet on the development of Oppia nitens (Acari,Oribatei )an d on themicroflor a ofit salimentar ytract .Pedobiologi a21 ,202-210 . Swift M.J., Heal O.H. and Anderson J.M. (1979) Decomposition in TerrestrialEcosystems .Blackwell ,Oxford . TarmanK . (1968)Anatomy ,histolog yo forlbati dgu tan dthei rdigestion . Bioloski16 ,67-76 . Van der Drift J. (1951)Analysi s of the animal community in a beech forestfloor .Tijdschrif tvoo rEntomologi e94 ,1-168 . Van der Hammen L. (1952) The Oribatei (Acari) of the Netherlands. ZoölogischeVerhandelinge nLeide n17 ,1-139 . WallworkJ.A . (1958)Note so nth e feedingbehaviou r ofsom e forestsoi l Acarina.Oiko s9 ,260-271 . WallworkJ.A . (1967)Acari .I nSoi lBiology . (A.Burge san dF .Raw ,Eds ) AcademicPress ,London ,p p363-411 . Wallwork J.A. (1983) Oribatids in forest ecosystems. Annual Review of Entomology 28,109-130 . Walter D.E. (1987). Trophicbehaviou r of "mycophagous"microarthropods . Ecology68 ,226-229 . Walter D.E., Hunt H.W. and Elliott E.F. (1988). Guilds or functional groups?A nanalysi so fpredator y arthropods froma shor tgras sstepp e soil.Pedobiologi a31 ,247-260 . WoodringJ.P .an dCoo kE.F . (1962)Th ebiolog yo fCeratozete scisalpinu s Berlese, Scheloribates laevigatus Koch, and Oppia neerlandica Oudemans (Oribatei),wit ha descriptio no fal lstages .Acarologi a4 , 101-136. Woodring J.P . (1963) The nutrition and biology of saprophytic Sarcoptiformes.Advance s inAcarolog y1 ,89-111 . Zinkler D. (1970) Carbohydrasen streubewohnender Collembolen und Oribatiden. In Organismes du Sol et Production Primaire. IV. Colloquium pedobiologiae Dijon. (J.d'Aguilar , C.Athias-Henriot ,A . Bessard, M.-B. Bouché and M. Pussard, Eds) pp 329-334. Institute Nationald el aRecherch eAgronomique ,Paris .

81 Mites of different feeding guilds affect

decomposition of organic matter

SUMMARY.Th eimpac to frepresentative so ffiv efeedin gguild so foribati d miteso nmicrobia lrespiratio ndurin gdecompositio no f Avenella litterwa s studied.Herbivorou sgrazer sha dn oeffec to nmicrobia lrespiration ;herbo - fungivorous grazers andfungivorou s grazersha d astimulatin g effecto n microbialrespiration ,whil efungivorou sbrowser san dopportunisti cherbo - fungivoresha da ninhibitin geffec to nit .Th eguild swit hstimulatin gef ­ fectso nmicrobia lrespiratio nhav ei ncommo nth eabilit yt odiges tchitin , amai ncomponen t offunga lcell-walls .Chiti nconsist s ofnitrogen ,th e releaseo fwhic hma ystimulat efunga lgrowt han drespiration .Additio no f nitrogeni nexperiment sstimulate dmicrobia lrespiration ,bu tth epositiv e effecto fa herbofungivorou s grazercoul dno tb edemonstrate d inexperi ­ mentswher eextr anitroge nwa sadded .I ti sconclude dtha tstimulatio no f microbial respirationma yb e theresul to f thereleas e ofnitroge nfro m fungalcell-walls .Micro-arthropo dgrazin go nfung ii sdiscusse dwit hres ­ pectt oeffect so fmicro-arthropo d density,nutrien tavailabilit y inth e substrate andth enatur eo fgrazing .Nex tt othes eeffects ,tempora lan d spatialfactor sma yhav esom e influenceo nth eeventua lresul to ffunga l activityo noveral ldecompositio nrates .

INTRODUCTION

Inbot hcommunit y ecologyan decosyste mecolog yspecie sar eassemble di n groupsbase do nth esuppose dsimila rfunctio nexerte db yth especie swithi n agrou p(e.g .Hawkin s& MacMaho n1989 ,Walte re tal .1988) .I nanima leco ­ logy,Roo t(1967 )propose dth eguil dconcep tfo rsuc hgroups .Th econcep t ofguil dwa suse di nsoi lbiolog ysinc eSchuste r(1957 )define dmacrophyto ­ phages,microphytophage san dpanphytophage sbefor eth eter mguil dwa sas ­ signed to it.Als oBerthe t (1964),Lebru n (1971)an dLuxto n (1972)use d thisfunctiona lclassificatio no foribati dmite san dman yauthor sdi deve r

83 Microarthropodcommunitie s

since (e.g.Beha n& Hill ,1978 ;Kanek o1988 ;Wallwor k 1983).A tth etim e oftha tclassification ,th ecommo nopinio nwa stha tth efunctio no fsoi l faunai ndecompositio nwa smainl yfragmentation .Late rVa nde rDrif tan d Jansen(1977) ,Hanlo n(1981 )an dHanlo nan dAnderso n(1979 )mad eclea rtha t thegrazin go ffung icoul dals ob ea predominan tfunctio no fmicro-arthro ­ podsi ndecompositio no forgani cmatter . Manyquestion sstil lar et ob eanswered .Ho wi sdecompositio no forgani c matteraffecte db yth especie sabundanc ean ddistributio no ffungi ,b yden ­ sityan dag eo fmycelium ,b ysubstrat ephysica lan dchemica lproperties , byexten tan dperiodicit yo fsoi lmoistur ean dfinall ywha ti sth eprecis e roleo fmicro-arthropods .Fungu sfeedin gCollembol aca nalte rth ecompeti ­ tionbetwee n fungal species and consequently alter decomposition rates (Newell 1984b),whe non eo fthe mi stoxi co runpalatabl efo rth ecollem - bolan(Parkinso ne ta l1977 ,1979) ,o rwhe nth evertica ldistributio no f one of the fungus species extends the range of the collembolan (Newell 1984a, 1984b). Highdensitie s ofmicro-arthropod s tend toovergraz eth e fungian ddecreas edecompositio nrate s (Hanlon& Anderso n1979) ,bu thig h substrate quality permits a strong growth of fungiwhic h isno teasil y overgrazedb ymicro-arthropod s(Hanlo n1981) .Interestin gals oi sho wfung i aregrazed ,i sal lfunga lmateria ldigeste do rar esom epart slef tuntou ­ chedwhic hma yeventuall yaccumulate ? InChapte r4 iti sargue d thatth ecurren t classification offeedin g guildso fnon-predator ysoi lmite swa sno tsuitabl et oclarif ythei rpre ­ ciserol ei ndecomposition .T oreplac eth ecurren tfeedin gguild sa classi ­ ficationwa spropose dbase do ndigestin gabilitie so fth especies .Carbo - hydraseenzym eactivitie sforme dth ebasi so ffiv emajo r(species-rich )an d twomino rcategorie samon goribati dmites .Th efiv emajo rcategorie sare : herbivorousgrazers ,herbofungivorou sgrazers ,fungivorou sgrazers ,fungi - vorous browsers and opportunistic herbofungivores. The most important differenceo fthes efeedin gguild swit hth epreviousl yuse dmicro- ,macro- , andpanphytophage si sth edistinctio ni ndigestio no ffunga lcell-content s only (browsers)o ro fbot hfunga lcell-content san dcell-wall s (grazers). Inthi spape rw edemonstrat e theinfluenc eo frepresentative so feac h ofth efiv emajo rfeedin gguild so nth eproces so fdecompositio no forgani c matter.Ou rhypothesi si stha tth eherbivorou sgrazer swil lhav en oinflu ­ enceo ndecompositio nrate san dtha tth efou rguild sfeedin gi na specifi c wayo nfung iwil laffec tdecompositio nrate sguild-specific .Specie sdiges ­ tingfunga lcell-content sonl yma yhav ea les sstimulatin go reve ninhibi ­ tingeffec to nmicrobia lrespiratio n(fungivorou sbrowsers ,opportunisti c herbofungivores),whil especie sdigestin gbot hfunga lcell-wall san dcell - contentsar ethough tt ostimulat emicrobia lrespiratio n (fungivorousan d herbofungivorousgrazers) .Th elatte rspecie sma yreleas enitroge nfro mth e chitin in the fungal cell-walls, and can digest also inactive fungal

84 Effecto ndecompositio n

material, which may increase microbial growth rate. Both release of nitrogen inou rexperiment sa sNH4NO 3a swel la sadditio no fa cell-wal l digestingspecie sma yresul ti na stimulatio no fmicrobia lrespiratio ni n agedmycelium . Effectswil lb e interpreted fromou rknowledg e ofenzym e activities inth egut so fth especie suse d (Chapter4) .

MATERIALSAN DMETHOD S

Miteswer esample dfro msoi lan dmos score susin gTullgren-extractio nwit h wateri nth ecollectio njars .Th ejar swer echecke ddail yfo rth especie s tob euse di nth eexperiments .Fiv eoribati dmit especie swer euse di nth e experiments representing the fivemajo r feeding guilds (Chapter 4); the herbivorousgraze r ParachipCeria punctata (Nicolet1855 ), th eherbofungi - vorous grazer Nothrus silvestris (Nicolet 1855), the fungivorous grazer Punctoribates punctum (CL.Koc h1840) ,th efungivorou sbrowse r Chamobates borealis Trägärdh 1902 and the opportunistic herbofungivore Carabodes labyrinthicus (Michael1879) . The number ofmite s usedpe r experiment depended on the size ofth e mite. Inever y experiment 0.5m gadul tmite swer eused .Fo r P. punctata thiscorresponde dwit h1 5individuals ,fo r N. silvestris with11 ,fo rP . punctumwit h50 ,fo r C. borealis with6 0an dfo r C. labyrinthicus with12 . Themite swer eplace di na smal lja r( 5c mdiameter )o n6 g (dr ymass )sub ­ strate.Th ejar swer ecovere dwit ha gauz eo f4 0 pmmes hsize . The substrate was composed of 78% quarts sand (particle size 200- 800 pm),2 %illit ean d20 %pulverize dshoot so fth egras s Avenella flexuosa (L.)Dreye r (- Deschampsia flexuosa (L.) Trin.) .Th epulverize dgras swa s composedo f32.4 %+ 0. 1 lignin,26.6 %± 0. 1hemicellulos ean d32.6 %+ 0. 5 cellulose by mass, analyzed according toGoerin g and Van Soest (1970). Totalamount so fN ,P ,an dK were :3.1 %±0.1 ,0.2 %±0. 0 and2.4 %± 0.1 , respectively.Pulverizatio no forgani cmatte rwa sdon et oexclud epossibl e fragmentationeffect so fmite so nth eorgani cmatter .Funga lspecie swer e introducedwit h theorgani cmatter ,th especie scompositio no ffung ii s

therefore unknown,whic hma y result insomewha t different levels of C02 productionamon gserie so fexperiments .Nematode swer eno tpresen ti nth e jars.Bacteri aan dprotozoan swer epresent ,thei rrol ei ssuppose dt odomi ­ nateth einitia lstag ei nth eexperiment s (breakdowno fsimpl esugars) . Atth estar to fth eexperiment ,th esubstrat ei nth esmal lja rwa smois ­ tenedwit hde-ionize dwater ,mite swer eadde dan dth esmal lja rwa splace d withanothe ron econtainin g1 0m l0.1 NKO Hsolutio no nwe tfilte rpape rt o obtainhig hmoistur econdition sint oa bigge rja r( 11 )whic hwa shermeti -

85 Microarthropodcommunitie s

callyclosed .C0 2productio nwa smeasure di nth esmal lja rwit hKOH ,whic h wasreplace dtw otime spe rweek .Titratio nwit hHC lreveale dtota lamount s of C02produce d (Doelman& Haanstr a 1979),blanc swer euse d to tareth e titration.Th etota lamoun to fC0 2pe rthre eo rfou rday swa scalculate d 1 toC0 2production.h^.g" organi cmatter .Jar swer ekep ta t1 5°C . Eachserie so fexperiment sconsiste do fa ja rwit hsubstrat ean dmite s anda ja rwit hsubstrat eonl y(control )whic hwer ereplicate dfiv etimes . Theblank s (jarswithou tsubstrat ean dwithou tmites )i never yserie so f experimentswer ereplicate d threetimes .

Insom elate rserie so fexperiment snitroge nwa sadde da sNH AN03(Gam s _1 et al. 1987)t o anamoun t of 2g NH 4N03.1 . Inthes e experiments 40 ßl NH4NO3wa sadde da teac hreplacemen to fKOH-jars ,i ntota l8 times .Adde d nitrogena tth een dwa s22 4 pg Npe rjar .Tota lnitroge npe rja ri sabou t 37.2mg ,thu sth eadde dnitroge ni sles stha n1% . Differenceswer e tested forsignificanc e by analysis ofvarianc e(F - test).A smeasurement so frespiratio ni na time-serie sar eno tindependent , thelas tperio do fC0 2productio nwa suse donl yt odecid ewhethe rdifferen ­ cesbetwee ncontro lan dtreatmen twer estatisticall ysignificant .Calcula ­ tionsmad e onearlie rperio d shouldb e considered as indicative forth e starto fdivergenc eo fcontro lan dtreatment .W eteste dfo rdifference si n

C02productio na slat ea spossibl ei nth eexperiments ,becaus ethi sstag e mayreflec tth efiel dsituatio nmor etha na noveral ltes to ntota lrespira ­ tionwhic h includesth einitia lstage .

RESULTS

Theherbivorou s grazer, Parachipteria punctata, hadn oeffec to nth eC0 2 production (Fig.5.1a) .I tca nb econclude dtha tthi smite ,whic hi sno t able to feed on fungi, does not affect the rate of decomposition of

Avenella leaves.C0 2 production ofth emite s themselves,a sa resulto f feedingo nth eorgani cmateria li snegligibl ecompare dt oth emicrobia lC0 2 productiont ob emeasured .Bot hspecie sdigestin gfunga lcell-walls ,th e herbofungivorous grazer, Nothrus silvestris, andth efungivorou sgrazer , Punctoribatespunctum, hada neventua lpositiv eeffec to nth edecompositio n rate:i nth epresenc eo fth emite sC0 2productio nwa shighe rtha ni nthei r absence(Fig .5.1b ,d) .Th etw ospecie showever ,no tabl et odiges tfunga l cell-walls,th efungivorou sbrowser , Chamobates borealis, andth eopportu ­ nisticherbofungivore , Carabodes labyrinthicus, appearedt ohav ea neven ­ tuallynegativ e effecto nth edecompositio nrate :i nth epresenc eo fth e mitesC0 2productio nwa slowe rtha ni nthei rabsenc e (Fig.5.1c ,e) .

86 Effect on decomposition

® Parachutera punctata y u Nothrus sivestris ® Punctoribates punctun

ff« yj LU i Carabodes labyrinthicus Chamobates boréals

II. y i I Days

Figure 5.1. C07 production from pulverized Avenella leaves in the absence (white bars) and the presence (black bars) of (a) Parachipteriapunctata , a herbivorous grazer, (b) Nothrussilvestris , a herbofungivorous grazer, (c) Carabodes labyrinthicus, an opportunistic herbifungivore, (d) Punctoribatespunctum , a fungivorous grazer and (e) Chamobatesborealis , a fungivorous browser. Asterisks above the bars of the last measurement reflect the statistical significance of difference: *, **; p<0.05 resp. p<0.01. Asterisks above earlier bars are to be considered as indicative for the start of divergence between treatment and control as they are not independent.

87 Microarthropod communities

Itca nb econclude d that fungivory ofmite saffect s C02production .Th e

one herbivorous mite had no effect on C02 production, unlike the four fungivorous mites. But the nature of the effect is completely different between grazers (herbofungivorous and fungivorous grazers) and browsers (fungivorous browsers and opportunistic herbofungivores) as explained in Table 5.1.Mite s that candiges tchiti nha da positiv e effecto nmicrobia l respirationan da sa consequenc e ondecompositio n rate;mite swithou t that capacity had anegativ e effect.

Table 5.1. Cellulose, trehalase, and chitinase activities of representatives of five feeding guilds ofmite s and their effects on decomposition rate.

cellulase trehalase chitinase effect on feeding activity activity activity decompos. guilds rate

Parachipteria herbivorous punctata grazer

Nothzvs herbofungivorous silvestris grazer Punctoribates fungivorous punctum grazer

Carabodes opportunistic labyrinthicus herbofungivorous Chamobates fungivorous borealis browser

88 Effect on decomposition

.® Nothrus slvestris added attar 2t days

Lii1« 20 2H 2i*i 26 ii

> ® NH4N03 added after 17 days j

'a

I J •a

12 14 16 16 20 22 24 26 11

5 ISlothru s slvestris

ati * NH4N03

i 'o>

1 llu 1ia N » » S H Days

Figure 5.2. C02 production from pulverized Avenella leaves (a) in the absence (white bars) and the presence (black bars) of Nothrussilvestris , a herbofungivorous grazer, added after 21 days, (b) without (white bars) and with (black bars) NH^N03added after 17 days and (c) with added NH^N03 in the absence (white bars) and the presence (black bars) of Nothrus silvestris. For the meaning of asterisks see legend of Figure 5.1.

89 Microarthropodcommunitie s

So,mite sdigestin gfunga lcell-wall sa swel la scell-content shav ea possiblypositiv efee dbac ko nmicrobia lactivity .Mite sfeedin go ncell - contents onlyhav e anegativ e effect on fungal activity.Th e effecto f fungivorous grazers or herbofungivorous grazers on a senescent fungal community is demonstrated in Figure 5.2a. In the presence of Nothrus

silvestris, a herbofungivorous grazer, added after 21 days, the C02 productionwa ssignificantl yhighe rtha ni nth eserie swithou tmites .Cell - wall digestionb y mites mayhav e apositiv e feedback on fungalgrowth . Chitin is an important component of the fungal cell-wall, and canb y definitionb edigeste db yfungivorou san dherbofungivorou sgrazers . Chitincontain so fabou t7 %N b ymass .I fi ti sth enitroge nfro mchiti n whichstimulate smicrobia lrespiration ,additio no favailabl eN mus thav e acomparabl epositiv eeffect .Figur e5.2 bdemonstrate sth eeffec to faddi ­

tiono fsmal lamount so fNH 4N03a tinterval so fthre eo rfou rday sfro mda y 17onwards .Eventuall ythi sadditio nha da positiv eeffec to nfunga lacti ­ vity,becaus e C02productio nwa ssignificantl yhighe ra tda y31 .S obot h additiono fa herbofungivorou smite ,whic hdigest schitin ,an dadditio no f

NH4N03 increased decomposition, probably by stimulation of microbial respiration. If extra nitrogen is the clue in the stimulation of microbial

respiration, thenadditio n ofNH 4N03 during thewhol e experiment should overshadowth epositiv efeedbac ko fth egrazin go fmites .Th enegativ eef ­ fect of fungivory should remain asha s been shown in the browser case (Chamobates borealis, Carabodes labyrinth reus Fig.5.1c ,e ). Figur e 5.2c

presentsresult sfro mth efina lexperimen twit hregularl yadde dNH 4N03i n smallamount si njar swit ho rwithou tgrazers .Afte rthre eweeks ,a perio d comparablet oth efirs tserie so fexperiments ,Nothru ssilvestri sha dane ­ gative influenceo nmicrobia l respirationan dthu so ndecompositio nrat e

inth epresenc eo fadde dNH 4N03. Weconclud etha ti tdepend so nth eassimilatio nefficienc yo fth emite s

for nitrogen whether or not feeding on fungi stimulates C02 production rates.Furthermore ,th epositiv efeedbac ko ftw ograzer s( afungivorou san d aherbofungivorou s one)ca nb e explained frommakin gnitroge navailabl e throughdigestio no fchitin ,a mai ncomponen to fth efunga lcell-wall .

DISCUSSION

Ourchoic et oexpres smit edensit yi nm gmite si son eou to fsevera lpossi ­ bilities.Th emai npoin ti swhethe rthi schoic einterfere swit hth efina l resultso rnot .Bot ha larg especie s (Carabodes labyrinthicus) anda smal l

90 Effecto ndecompositio n one {Chamobates borealis) result in a negative influence on microbial respiration. Positive influence was found also inbot h a large species (Nothrus silvestris) anda smal lon e (Punctoribates punctum). So,siz eo f themites ,o rnumber si nth eexperiment sprovid en oalternativ eexplanatio n forth eresult sobtained .Anothe rexpressio nfo rth eimpac to fmite sma y bethei rmetaboli cactivity .Th esequenc eo fmetabolicall ymos tactiv e(a s measured by 02 consumption at 10 0C)mite s in descending order is: C. borealis, P. punctum, P. punctata, N. silvestris, C. labyrinthicus (data fromBerthe t(1964) ,Luxto n(1975) ,Web b(1969 )an dWoo dan dLawto n(1973 ) onth eliste do rclosel yrelate dspecies) .Agai nthi ssequenc eprovide sn o alternativeexplanatio nfo rth efina lresults .Thu sth edensit yo fmites , throughth eleve lo ftota lmetaboli cactivity ,doe sno texplai nth eoutcom e ofth eexperiments . The differences obtained between our series of experiments in the absoluteleve lo fmicrobia lrespiratio nma ydepen do nsmal ldifference si n substratequality ,o ri nmicrobia lspecie scomposition .W ehav echose nt o useth enatura lmicrobia lspecie sassemblag epresen to nth eorgani cmatte r tob esur etha tth eorgani cmatte rform sth eappropriat esubstrat efo rth e microflora and themit especie sma yb efamilia rwit h the fungi ini ta s theyorginat e all fromlitte r inwhic h Avenella leaves arepresent .Th e alternative:additio no ffe wculture dfunga lspecie sha sth eadvantag etha t microbialrespiratio n ismayb emor eprecisel y reproduced amongserie so f experiments,bu tha sth eris ktha tth eintroduce dfung iar eno tth ebes t decomposerso fth eselecte dorgani cmatte ro rmayb eunpalatabl et oon eo f theselecte dmit especies . Feedingo foribati dmite so nfung ica nlea dt oeithe ra stimulatio no r aninhibitio no fdecompositio ndependin go nth enatur eo ffeeding .Digesti ­ ono ffunga lcell-wall snex tt ocell-content s (grazing)lead st ostimula ­ tion,digestio n ofcell-contents _onl y (browsing)lead s to inhibitiona t equaldensitie so fmite sexpresse di nm gmit epe rg organi cmatter .Hanlo n andAnderso n(1979 )showe dtha tdensit yo fth ecollembola n Folsomia Candida influenced decomposition rate. High densities resulting in overgrazing inhibited0 2consumptio n (whichi sequivalen t toC0 2productio nan dthu s decomposition inou r experiments),whil e lowdensitie s had theopposit e effect.Furthermore ,Hanlo n(1981 )demonstrate dtha tfung igrow na thighe r nutrientlevel swer estimulate db ycollembola nfeeding ,whil efung igrow n atlowe rlevel swer einhibited .S ofar ,thre efactor sinfluencin gmicrobia l respirationunde rfeedin go fmicro-arthropod shav ebee ndistinguished :th e natureo ffeeding ,th edensit yo fmicro-arthropod san dth enutrien tleve l ofth esubstrate .Th eeffect so fthes efactor sar eclosel ylinked .Micro - arthropodgrazin go nfung iha sa negativ eeffec tfo rfung ib ydamagin gan d decreasingfunga ltissue snex tt oa positiv eeffec tb yreleasin gminerals , e.g. nitrogen,whic hma y result ina faster fungal growth.Th ebalanc e

91 Microarthropod communities betweenth etw oeffect sdetermine sth efina lresult .Grazer sma yleav eles s damagedtissue sa sthe ydiges talmos tal lo fth efunga ltissue seaten ,con ­ trary to browsers which digest only fungal contents and thus will leave more damaged fungal tissue.Moreove r grazerswil l also releasemor emine ­ rals from senescent fungal tissues compared tobrowser s and in this way stimulatefunga lgrowth .Micro-arthropo ddensit yan dnutrien tavailabilit y for themicroflor a determine thebalanc ebetwee ndecreas e and increase of microbial biomass. A high micro-arthropod density leads to an increased fungaldestructio nan dthu st olowe rrespiration .A hig hnutrien tavailabi ­ lity leads to a high fungal growth rate and consequently a more rapid recovery from grazing damage and thus ahighe r respiration. In Table 5.2 possibleoutcome so finteraction so fth enatur eo fmicro-arthropo dfeeding , micro-arthropoddensit yan dnutrien tavailabilit yar ehypothesized .I nthi s table stimulation of microbial respiration ismor e frequent with grazers thanwit hbrowsers ,a t lowmicro-arthropo ddensitie s thana thighe r ones, and athighe r nutrient availabilities than at lower ones.

Table 5.2.Hypothetica l outcomes of the combined effects on microbial respiration of the nature of grazing (grazer or browser), density of fungal feeding microarthropods and nutrient availability for fungi.

nature of density of nutrient possible effect grazing microarthropods availability on fungal respiration

high high grazer low high low ++ low + high high browser low high low low

92 Effecto ndecompositio n

Patchinessi nfunga ldistributio no nth esubstrat elead st oalternatin g highan dlo wgrazin gpressur eo fmicro-arthropod san dma yeventuall yresul t in an overall stimulating effect on microbial respiration (Bengtson & Rundgren1983) .Spatia lan dtempora leffect swhic hma yb eo fmino rimpor ­ tancei nsmal lscal emicrocos mexperiment sca nb ever yimportan ti nnature . Anillustratio nma yb ea microcos mexperimen ti nwhic hseedling sar egrown . Assuming that the seedling takes advantage of the nitrogen releasedb y micro-arthropodgrazing ,thi snitroge ni sno tavailabl efo rpositiv efeed ­ backo nmicrobia lrespiratio na sargue dbefore ,henc ea stron guptak eo f nitrogenb yseedling swil linhibi tth edecompositio nprocess ,resultin gi n anunmeasurabl eeffec ti nseedlin ggrowth .Whe nther ei sn ostron gnitroge n uptakeb yseedlings ,a measurabl eeffec to nseedlin ggrowt hca nals ohardl y be expected. Bàâthe t al. (1981)foun dn o difference ingrowt ho fpin e seedlingsi nth eabsenc ean dpresenc eo fmicrobia lfeedin gnematode san d mites.Kuikma nan dVa nVee n (1989),however ,demonstrate da 65 %increas e inmineralizatio nan dplan tuptak eo fbacteria l15 Ni na microcos mexperi ­ mentwit hbacteri aan dprotozo aa scompare dwit hbacteri aonly .

REFERENCES

Bàâth,E. ,U .Lohm ,B .Lundgren ,T .Rosswall ,B .Söderströ m& B .Sohlenius , 1981. Impacto fmicrobial-feedin ganimal s ontota lsoi lactivit yan d nitrogendynamics :a soi lmicrocos mexperiment .Oiko s37 ,257-264 . Behan, V.M. & S.B. Hill, 1978. Feeding habits and spore dispersal of oribatid mites in the North American arctic. Revue d'Ecologie et Biologied uSo l15 ,497-516 . Bengtsson, G. & S.Rundgren , 1983.Respiratio n and growth of afungus , Morteriella isabellina, inrespons e tograzin gb yOnychiuru s armatus (Collembola).Soi lBiolog yan dBiochemistr y 15,469-473 . Berthet, P., 1964. L'activité des Oribatides (Acari: Oribatei) d'une chênaie.Mémoire sInstitut eRoya lde sScience sNaturelle sd eBelgiqu e 152,1-151 . Doelman,P .& L .Haanstra ,1979 .Effect so flea do nth edecompositio no f organicmatter .Soi lBiolog yan dBiochemistr y 11,481-485 . Drift,J . van der & E.Jansen , 1977.Grazin g of springtails onhypha l mats and its influence on fungal growth and respiration. Ecological Bulletin25 ,203-209 . Gams, W., H.A . van der Aa, A.J. van der Plaats-Niterink,R.A . Samson, J.A. Stalpers, 1987. CBS course on mycology. 3rd edition. Centraal Bureauvoo rSchimmelcultures ,Baarn ,Th eNetherlands . Goering,H.K .& P.J . vanSoest ,1970 .Forag e fiberanalysi s (apparatus, reagents, procedures, some applications). Agricultural Handbook 379 USDAARS . Hanlon,R.D.G . &J.M . Anderson,1979 .Th eeffect s ofCollembol agrazin g

93 Microarthropodcommunitie s

onmicrobia lactivit yi ndecomposin glea flitter .Oecologi a38 ,93-99 . Hanlon,R.D.G. ,1981 .Influenc eo fgrazin gb yCollembol ao nth eactivit y of senescent fungal colonies grown on media of different nutrient concentration.Oiko s36 ,362-367 . Hawkins,C.P .& J.A .MacMahon , 1989.Guilds :th emultipl e meanings ofa concept.Annua lRevie wo fEntomolog y 34,423-451 . Kaneko,N. ,1988 .Feedin ghabit san dchelicera lsiz eo foribati dmite si n cooltemperat e forestsoil s inJapan .Revu ed'Ecologi e etBiologi ed u Sol25 ,353-363 . Kuikman,P.J . &J.A .va nVeen ,1989 .Th e impacto fprotozo ao n theava i lability of bacterial nitrogen to plants. Biology and Fertility of Soils8 ,13-18 . Lebrun, Ph., 1971. Écologie et biocénotique; quelques peuplements d'arthropodes édaphiques. Mémoires Institute Royal des Sciences Naturellesd eBelgiqu e165 ,1-200 . Luxton,M. , 1972.Studie s on the oribatid mites ofa Danishbeec hwoo d soil.I .Nutritiona lbiology .Pedobiologi a12 ,434-463 . Luxton,M ., 1975 .Studie s onth e oribatid mites ofa Danis hbeec hwoo d soil.II .Biomass ,calorimetry ,an drespirometry .Pedobiologi a15 ,161 - 200. Newell,K. ,1984a .Interactio nbetwee ntw odecompose rbasiodiomycete san d acollembola nunde rsitk aspruce :distribution ,abundanc ean dselectiv e grazing.Soi lBiolog yan dBiochemistr y 16,227-233 . Newell,K. ,1984b .Interactio nbetwee ntw odecompose rbasiodiomycete san d acollembola nunde rsitk aspruce :grazin gan dit spotentia leffect so n fungal distribution and litter decomposition. Soil Biology and Biochemistry 16,235-239 . Parkinson,D. , S.Visse r& J.B .Whittaker ,1977 .Effect so fcollembola n grazingo nfunga lcolonizatio no flea flitter .In :Loh mU .& T .Persso n (eds)Soi lorganism sa scomponent so fecosystems .Ecologica lBulletin s 25,75-79 . Parkinson,D ., S .Visse r &J.B .Whittaker , 1979.Effect s ofcollembola n grazing on fungal colonization of leaf litter. Soil Biology and Biochemistry 11,529-535 . Root,R.B. , 1967.Th enich e exploitation pattern of the Blue-grey Gnat catcher.Ecologica lMonograph s37 ,317-350 . Schuster,R. ,1956 .De rAntei lde rOribatide na nde rZersetzungsvorgänge n imBoden .Zeitschrif tfü rMorphologi eun dÖkologi ede rTier e45 ,1-33 . Wallwork, J.A., 1983.Oribatid s in forest ecosystems.Annua l Reviewo f Entomology28 ,109-130 . Walter, D.E., H.W. Hunt & E.T. Elliott, 1988. Guilds or functional groups?A n analysis ofpredator y arthropods froma shortgras s steppe soil.Pedobiologi a31 ,247-260 . Webb, N.R., 1969. The respiratory metabolism of Nothrus silvestris Nicolet.Oiko s20 ,294-299 . Wood,T.G . &J.H . Lawton,1973 .Experimenta l studieso n therespirator y rateso fmite sfro mbeech-woodlan dlea flitter .Oecologi a12 ,169-191 .

94 Coexistence in soil microarthropods

SUMMARY. Aspatia lmode l ispresente d toevaluat e thebalance san dcompen ­ satoryeffect sbetwee nlife-histor y traits,efficienc yo fus eo fresources , andtoleranc e forshort-term ,unpredictabl e environmentalextreme s insoi l microarthropods.I tappear stha tnon-resource-relate d life-historytraits , sucha smobility ,ca ncompensat e forles sefficien tus eo ffood , resulting in the model in coexistence of more species than the number of available resources.Th ecompetitiv eexclusio nprincipl eappear st ofai lwhe nmobili ­ ty of the competing species isno tunlimited . The question inecolog y why are soman y speciespresen t ona small scale should therefore be:wh y are so few species present where there appears tob e room formore .

INTRODUCTION

Speciesdiversit y insoi lmicroarthropod s (mitesan dspringtails )i susual ­ ly very high. Moritz (1965) found on average 33 oribatid species per 500 cm2 (range 23-45) inCentra l European forest soils.Siepe lan dVa nd eBun d (1988) found on average 45 oribatid species per 250 cm2 (range 37-52) in unmanagedDutc hgrasslands .Fo ral lsoi lmicroarthropod sthe yfoun do nave ­ rage10 8specie spe r25 0cm 2.Karppine n (1958)reporte dfro mFinnis h forest soilsa naverag eo f1 9oribati d species (range8-26 )o na slittl e as5 cm 2. All samples were taken up toa dept h of 5cm . Thishig h species diversity ona ver ysmal lscal e seemst ob ea todd swit hth enich econcep t formulated byHutchinso n (1957)an dSchoene r (1989),whic himplie stha tspecie sshoul d minimizenich eoverla p inorde rt osurviv e interspecificcompetitio n (Har­ din 1960,Arthu r 1984). So there should either be many resources in soil ona smal l scale,distinguishabl e formicroarthropod s (Anderson 1975), or microarthropods,belongin g todifferen tspecies ,shoul db eabl et ocompen -

95 Microarthropod communities sate for inefficientus e of,o rno thavin g access to,resource swit h (com­ binations of)othe r traits such asmobility , fecundity, spreading inovi - position,o rtoleranc et oshort-ter munpredictabl eenvironmenta lextremes . To evaluate thepossibl e compensation of inefficient use of,o r access to, resources by certain life-history traits,a simulationmode lwa scon ­ structedwhic h allowedsoi lmite s tomov e freely overa gri dan d tous e at most two types of food. It was hypothesized that an inefficient user of foodca n survivewhe n itmove s faster,o rwhe n it ismor e tolerant forpe ­ riods of food shortage than an efficient user of food. Eventually, many specieswer ehypothesize d tob e able tocoexis t on only two foodsources . Existinghypothese s on the coexistence of species sucha s thecompeti ­ tiveexclusio nprincipl e (Hardin1960 )an dHuston' s (1979)genera lhypothe ­ siso nspecie s diversity arediscusse d inligh to fth esimulatio nresults .

DESCRIPTION OF THE MODEL

A model with 132x120 grid cells was constructed. For each grid cell the following parameters were defined: probability ofdrought ,probabilit y of heat,probabilit y of frost (meant as suddenoccasions ,no t as predictable events inth eseason )an dpossibilit y ofvertica lmigratio n toescap e from thesehazard s (forsmal lspecie s only).Th eenvironmenta l factorswer ede ­ fineda sa gradien to nth egrid ,fro ma probabilit y ofmaxima l10 %pe r time step to 0% in steps of 1% per 8 rows or columns of grid cells (leaving about one third of the field unaffected). Nex t to the abiotic factors a biotic component, food, was defined for each grid cell. Food was offered in two independent forms. Amount of fungi was defined inunit s F, and in each grid cell F followed, independent of neighbouring grid cells, the growth function:

Ff * KP

rf Ft + (KF-Ft)* e- whereK Fi sth ecarryin gcapacit yo ffung ian dr Fth e intrinsic growth rate of fungi. Initial values (Ft) for all grid cells were set at 6.0. The second foodsourc ewa s organicmatte r fromgree nplant s andalgae 1i nwhic h two functions were defined. Algal growth was defined, and enlarged with annually falling leaves,as :

96 Coexistence

0t * Ko + 0A * K^asz-to) 10 0t + (Ko-0t) * e"

where 0 isorgani cmatte r from greenplant s andK gan dr 0ar e theircarry ­ ingcapacit yan dintrinsi cgrowt hrate ,respectively .A secon dinpu to for ­ ganic matter on the soil surface was the annually (ICt^^-tp)) falling leaves (deadorgani c matter): 0A,whic h coincidedwit h mite reproduction. Timestep swer eweeks ,t oallo wfutur ecomparison swit hexperimenta ldata . The initial number of miteswa s set at onehunder d per species spread over the grid at regular distances. Individuals of second, third, etc. specieswer e placed inneighbourin g grid cells, initially. This resulted ina reproducibl e starto fal l simulations, initial equal availability of resources for all competing species, and competition all over the grid. Mites feeding inth egri dcell swer egroupe d inguild s (Chapter 4). Six feeding guilds occurred in the model: herbivorous browsers (eating 0.2 units 0 per time step), herbivorous grazers (0.1 units 0),fungivorou s browsers (0.2unit sF ),fungivorou sgrazer s(0. 1unit sF ), herbofungivorou s grazers (bypreferenc e 0.05 units Fan d0.0 5 units0 ,bu t ifeithe ron eo f those is absent 0.1 units F or 0.1 unit 0) and finally the opportunistic herbofungivores (by preference 0.2 units F, but in the absence of F the sameamoun t of0 ). Grazer s ate less thanbrowser s because of their better enzymatic digestion capacity (they are able to digest cell walls next to cell-contents). The amount of foodwa s eaten at each time step. However, when the amount of food was insufficient (less than the amount defined above) for then th mite in the grid cell, mites from n onma y starve.Th e probability of deathb y starvationwas :

VA = 1 -exp( - ln2 / LD50)

per timestep ,wher e LD50 isth enumbe ro fweek s afterwhic hhal fth epopu ­ lation ofmite s died from starvation inexperiments .Th e order of feeding for competing species was at random at every time step per grid cell.

Reproduction tookplac e onceever y 52tim estep s (oneyear) , att 0,an d waschose n tob e thelytokous,tha t isever ymit ewa sa femal e andgav efe ­ male offspring only. Egg-laying was either semelparous, all at once, or iteroparous following the functions:

Rt - Fct (1 - e-***) and

Fct+1 = Fct -R t

97 Microarthropod communities

whereR t isreproductio n at time t (weeks), Fct future reproductionpoten ­ tial at time t and x is the parameter of iteroparity, the smaller x the more iteroparous the reproduction willbe . The whole grid consisted of 132x120 cells.Mite s were allowed to move from one grid cell to another. Individual mobility has been defined for randomwal k orphoresy . The randomwal k type let themit emov e to theor ­ thogonallyneighbourin ggri dcells .Th eexten to fthi styp eo fmobilit ywa s scaledfro m1 0t o100% ,i nstep so f10 %probabilit yo factua lmovement .Th e direction of the movement was random, because there is little evidence that soilmite s head towards distant foodsources . The phoresy type ofmobilit y let themit e move toan y grid cell inth e model.Th eprobabilit y toge tt oa certai ngri dcel ldepende do nth eamoun t of food present at the grid cell; a cellwit h a five times higher amount of food had an equally higher probability tob e reached. The probability mightb e small,bu tneve r zero.Thi snon-rando m direction ofmovemen t was derived fromth edirectiona lmigratio n tone wfoo dsource so fth ecarrier s ofth ephoreti cmites ,mostl yflyin ginsects .Thes einsect sar eeithe rabl e to locate a distant food source or the mites leave the carrier only on a favourable spot (Binns 1982). The phoresy modelled was adult carrier- unspecific phoresy as defined inChapte r 2. Tolerance toenvironmenta lextreme swa sdefine dpe rspecies .Th eproba ­ bility todi e from frost, drought orhea t depended on the probability of thehazar d to occur at the grid cell where the mite was located. Species might survive environmental uncertainty either by tolerating orb y avoi­ dance. Small species were defined able to avoid frost, drought and heat because they canmov e into deeper soil layers (Metz 1971). Theprobabilit y todie ,eithe rfro mstarvatio no rfro menvironmenta lex ­ tremes,wa s calculated for every grid cell per species per time step.Fo r every individual mite present in the grid cell, a random number was com­ paredwit hth ecalculate dprobabilit y todie ,resultin g inth edeat ho fth e mites with random numbers lower than the calculated probability. A listing of the simulation program is available from the author on request.

SENSITIVITY ANALYSES AND RESULTS

Food and feeding

Food availability determined the population sizes in the model. Increase

offoo da sdetermine ddepende do ntw oparameters :r Fo rr 0,th erat eo fin ­

crease, andK F or KQ, the carrying capacity, of fungi respectively algae.

98 Coexistence

The impacto fthes eparameter so nnumber so feithe rfungivorou so rherbivo ­ rousmite si sshow ni nFigur e 6.1fo rvariou svalue so fr Fo rr 0an di nFi ­ gure 6.2fo rvariou svalue so fK Fo rKQ . From these figuresi tca nb econ ­ cluded thatth erat eo fincreas eo ffood ,rathe r thanth ecarryin gcapaci ­ ty,determine d population size eventually. Thus food inthi smode l is al­ ways limited (andlimiting) ! Default values ofr F, -c0, KF,an dK Q forth e simulations tofollo war egive ni nTabl e6.1 .Th edefaul tmit e speciesi s artificialan di sconstructe do nth emos t simplean daverag e traitso fmi ­ tes.Eac htim este pi na figur erefer st oa naverag eo f1 0simulatio nruns .

11

10.

9 =0.2 0 =0.1 5 8 =0.1 0

7 -0.05

6. a £• 5 Ç

4

3

2

1

8 9 10

Figure 6.1. Population size during the first ten generations of a fungi­ vorous grazer at different values of the fungal growth rate (rf), or a herbivorous grazer at different values of increase of algae and organic matter (rom), both referred to in the figure as r.

Inth eforme rsectio ndifferen tfeedin gguild swer edefine do nth ebasi s of differences inth eamoun t offoo d used. Browsers were defined asles s efficientfeeder stha ngrazer san dsom eguild sexploite dbot hfung ian dal ­ gae.S oi ti st ob eexpecte dtha tth efeedin gguil dals odetermine sth epo ­ pulationsiz ei nsingl especie sruns .Figur e 6.3present spopulatio nsize s of species belonging to different feeding guilds. Browsers reached the

99 Microarthropod communities leasthig hnumbers ,grazer s reachedhighe rnumber san dabilit y tous etw o food types increased numbers even more forbot h thebrowse r type (oppor­ tunistic herbofungivore)an dth egraze r type (herbofungivorous grazer).

Table 6.1.Defaul t values used inth esimulatio n experiments.

Initial number ofmite s 100 Individual mobility 10 Feeding guild fungivorous grazer Growth raterf ,ro m 0.25 Carrying capacity KF,K O 9 Annual input oforgani c matter(0 ) 6 VA (chance todi ei nabsenc e offood ) 0.100 Reproduction (number ofeggs ) 36 Iteroparity parameter 5.00 (semelparity) Tolerance todrough t tolerant " "fros t tolerant " "hea t tolerant

11

10

9

8

7.

6 a £• 5_| Ç

4

3.

2

1

2 3 4 5 6 10 time

Figure 6.2. Population size during the first ten generations of a fungi­ vorous grazer at different values of the fungal carrying capacity (KF), or a herbivorous grazer at different values of the algal carrying capacity (KO), both referred to in the figure as K.

100 Coexistence

Theperio da specie scoul dliv ewithou tfood ,i.e .th eprobabilit yt o die(VA )i nth eabsenc eo fth erequire damoun to ffood ,ha dsom einfluenc e onpopulatio nsiz e(Fig .6.4) .Compared ,however ,t oth einfluenc eo ffeed ­ ingguil do rrat eo fincreas eo ffood ,V Aha da smal leffec to nnumbers .

11.

10. ^1 9 8_ 7.

Z 1 herbofungivorous grazer c5 2 opportunistic herbofungivore 3 herbivorous grazer 4 fungivorous grazer 4 5 herbivorous browser 6 fungivorous browser 3 2. 1

10

Figure 6.3. Population size during Che first ten generations of species belonging to different feeding guilds; fungivorous grazer, or browser, herbivorous grazer, or browser, herbofungivorous grazer, and opportunistic herbofungivore.

Individualmobilit y

Theparamete ro findividua lmobilit yo fth erando mwal ktyp erange dfro m 1t o10 ,i nstep so f10 %probabilit yo factua lmovement .Figur e6. 5pre ­ sentsequilibriu mpopulatio nsiz eversu sdegre eo fmobility .Difference s innumber sdu et odifference si nmobilit ywer eo fa comparativel y small magnitude.However ,combinatio no flo wmobilit yan dhig hV Aparamete rre ­ sultedi nsmal lpopulation s (offspringwoul dresul ti nloca lhig hdensi ­ ties,a depletio no ffoo dan dconsequentl ybecaus eo fth ehig hstarvatio n ratea minimu mo fsurvivor samon gtha toffspring) .

101 Microarthropodcommunitie s

Fecundity

Figure6. 6(lin e3 )demonstrate sequilibriu mpopulatio nsize sa tincreasin g fecundities.No tshow ni nthi sfigur ei stha tth eequilibriu mwa sreache d ata late rstag ea tlowe rfecundities .Th eshap eo fthi sfunctio ni srathe r peculiar:a sa matte ro ffac ti ti scompose do ftw ofunction s (Fig.6.7) . Survivalrate so fimmature sdepende do nloca ldensit yan dsurviva lrate s decreasedwit hincreasin gdensity ,becaus emobilit ywa slimite dt oorthogo ­ nalcell s(Fig .6.7 :lin eA) .A highe rloca lnumbe ro fimmature sincrease d theprobabilit ytha tsom emove drelativel yfa rfro mth eeg gdepositio npla ­ cean dincrease dthei rprobabilit yt osurviv e(Fig .6.7 :lin eB) .Togethe r bothfunction ssho wa di pa tmoderat e fecundities.Whe nmobilit ywa sse t tophoresy ,th edi pdisappeared ,du et oth edisappearanc e ofth ehighe r population numbers at low fecundities in case of restricted mobility (Fig.6.6 :lin e 2). Halvingth edefaul tmobilit yresulte d ina downward s rotationo flin eB i nFigur e6. 7whic hresulte di nth efunctio npresente d inFigur e6. 6 (line4) .

11., 10 VA=0.1 9. VA=0. 2 VA-0.3 VA.0.4 8 7 6 5. 4 3. 2. 1.

8 9 10

Figure 6.4. Population size during the first ten generations of afungi .- vorous grazer at different values of tolerance to food shortage (VA).

Iteroparity(spreadin govipositio ni ntime ;x-0.05 )resulte di nincrea ­ sedpopulatio nnumber sbecaus eloca linterspecifi ccompetitio ndecreased .

102 Coexistence

Thedi pa tmoderat efecundities ,however ,stil lexiste d(Fig .6.6 :lin e1) . Thisdi pvanishe dwhe nspreadin go fovipositio nwa sdefine dbot hi ntim e andi nplac e(whe nindiviudal swer eabl et ooviposi ti ndifferen tcell sa t differenttimes) .S ofecundit yinfluence dequilibriu mpopulatio nsize .Th e extentt owhich ,wa sinfluence db yiteroparit yo rsemelparit yan db yth e individualmobilit yo fth especies .

Abioticfactor s

Speciesi nth emodel ,intoleran t todry ,col do rho tcondition swer eno t present inarea so fth edefine dfiel dwher eth efrequenc yo fthes ehars h conditionsi nth egri dcell swa shigh .I narea shavin gmoderat efrequencie s ofan yo fthes ehars hcondition sintoleran tspecie sha da moderat epopula ­ tion density. As a result the area available was decreased for these species.

9.27

9.25.

9.23.

9.21 .

o 9.19. II 9.17. a. ç 9.15.

9.13.

9.11 .

9.09.

9.07.

9.05. 12 3 4 5 6 7 10 mobility

Figure 6.5. Equilibrium (t-10) population size of a fungivorous grazer at different values of individual mobility of the random walk type.

Interactiono ftw ospecie s

Thecompetitiv e rankingo fth esi xfeedin gguild sentail sfe wsurprises .

103 Microarthropod communities

The fungivorous grazerwa s abette r competitor than the fungivorousbrow ­ ser, because of the lower amounts of food the former ingested. The same held, mutatis mutandis, for herbivorous grazers and browsers. In general species able tous e twofoo d typeswer ebette r competitors thanthos econ ­ fined to only one. The herbofungivorous grazer was the best competitor. However, the opportunistic herbofungivore drived either fungivorous or herbivorous browsers to extinction, but had a stable coexistence with either fungivorous orherbivorou s grazers (stabilitydepende do nth erati o ofunit s Fan d0 whic h isdefault) . Thehig h demand for foodo f theoppor ­ tunisticherbofungivor e was compensated forb y itsabilit y tochang e food types and itcoul d coexistwit h a fungivorous grazer by feeding onalgae . It was able to coexist with a herbivorous grazer, because it preferred feedingo nfungi .S oa ninefficien tuse r offoo dma ycompensat ewit h other factors to coexist with the more efficient user of food.

10.0

9.9.

9.8-

9.7

9.6

0 9.5 II Z 9.4. £ CO 1 9.3

9.2.

9.1

9.0J

6 16 26 36 46 56 66 76 86 96 reproduction

Figure 6.6. Equilibrium (t=10) population size of a fungivorous grazer at different fecundities (3), the same when mobility is restricted (4), the same when mobility is unlimited (2), and when mobility is restricted and oviposition is iteroparous (1)•

In thenex t series of simulations a fungivorous grazer (the efficient user offood ) competed witha fungivorous browser.Th eextr a amounto ffoo d the browser ingested (defined as twice theamoun t ingested byth e grazer)

104 Coexistence

thebrowse ringeste d (defineda stwic eth eamoun tingeste db yth egrazer ) couldb euse di nsevera lways :a highe rfecundity ,a highe rmobility ,o r a longer starvationperiod . Inth e first serieso frun s theinefficien t usero ffoo d(th ebrowser )migh tcompensat ewit ha highe rfecundity .Figur e 6.8 demonstrates theoutcom eo fth ecompetitio n interm so flo grati oo f numbers (log(spl+l)/(sp2+l)) .Eve nwhe nth efecundit yo fth ebrowse rwa s onlya littl ehighe rtha nth egrazer ,i tha da ninitia ladvantag ebu teven ­ tuallyth egrazer swon .Onl ywhe nreproductio no fth ebrowse rwa sa tleas t twicetha to fth egraze ri tmigh tcoexis tfo ra longe rtim e(bu tno tinfi ­ nitely).Figur e6. 9present sth elo grati oo fgrazer san dbrowser swit hin ­ creasingmobilit y (randomwal ktype )o fth ebrowser .A ninitia ladvantag e ofth ebrowse rwa spresen twhe ni tmove da tleas tseve ntime sfaster .Per ­ manentcoexistenc ewa spossibl ewhe nth ebrowse rmove dnin etime sfaste r thanth egrazer .I nth ethir dserie so frun sth ebrowse rmigh tsurviv elon ­ geri nth eabsenc eo fth erequire damoun to ffood .Figur e6.1 0present sth e lograti oo fth epopulatio nsize si nthes eruns .Alread ywhe nth ebrowse r couldsurviv e1. 5 timeslonge rtha nth egraze r inth eabsenc eo fth ere ­ quiredamoun to ffoo di twoul dsho wbot ha ninitia ladvantag ean dpermanen t

reproduction

Figure 6.7. The combined effect of the local survival probability (a) with the probability of some individuals to move away (b), resulting in the function presented in Figure 6.6 (lines 1 and 3).

105 Mlcroarthropodcommunitie s coexistence.Whe ni twa sabl e tosurviv emor e thantwic ea slon ga sth e grazer,i twoul doutcompet eth egrazer .Th eparamete rV Aappeare dver yim ­ portanti ncompetition ,a resul twhic hcoul dno tb econclude dfro mth esen ­ sitivityanalysi si nsingl especie sruns .

8

7_

6.

5.

4.

£3 -

- 2

1.

-1.

S 6 8 9 10

Figure 6.8. The log ratio of numbers of a fungivorous grazer (spl) and a fungivorous browser (sp2) during the first ten generations ; fecundity of the browser varies from 1.00 to 2.67 times the one of the grazer.

SIMULATIONO FECOLOGICA LPRINCIPLE S

Huston'shypothesi so nspecie sdiversit y

Huston (1979)pointe dou ttha tunde rcondition so ffrequen tdisturbance s potentially competing species do notmanag e to reach such apopulatio n

106 Coexistence leveltha tspecie sma youtcompet eon eanother ,becaus e foodo rothe rre ­ sourcesar eno tlimiting .I nth emode la fungivorou s grazeran da fungi - vorousbrowse r competed forfoo dalon ga gradien to fincreasin gprobabi ­ lities of drought. Both the grazer and the browser were intolerant to drought and suffered from anincreasin g mortalityprobabilit y alongth e gradient. Moreover, when the fungivorous grazer reached its maximum populationdensity ,th ebrowse rwa soutcompete da sha sbee nshow nbefore . Figure6.11 b shows thenumber s atequilibriu m ofbot h speciesalon gth e gradient.Th e fungivorousbrowse rcoul d survive only inth epar to fth e gradientwher enumber s ofgrazer swer e loweredbecaus e of the increased probabilitieso fmortalit yan da tth esam etim eth eprobabilitie so f

7.

5_

_ 4 a. c3 .

-1.

6 7 8 9 10

Figure 6.9. The log ratio of numbers of a fungivorous grazer (spl) and a fungivorous browser (sp2) during the first ten generations ; individual mobility ratio of browser/grazer varies from 1 to 9.

107 Microarthropodcommunitie s mortality ofbot h species were still low enough to survive. So,thes e simulations support Huston's hypothesis on species diversity. When the browser isgive n twice ashig h amobilit y as thegrazer , it isabl et o extendit srang econsiderabl y (Fig.6.11c) .

4.

3.

2

1.

0.

•S -1. a iS =-2 .

-3.

-4.

-5,

-6.

-7

01 23456789 10 time

Figure 6.10. The log ratio of numbers of a fungivorous grazer and a fungi- vorous browser during the first ten generations; tolerance to food shortage of the browser varies from 1 to 4 times that of the grazer.

Identicalniche s

Themode lgive sth eopportunit yt ocompar especie sdefine dt ohav eidenti ­ calniches ,a sstate di nth ecompetitiv eexclusio nprincipl e(Hardi n1960) , evenwhe nthi sphenomeno nma yno texis ti nnatur e(Arthu r1987) .Th ecompe ­ titiveexclusio nprincipl ei sno tfalsifiabl ei nnatur ebecaus ean ydiffe ­ rencema ycaus especie scoexistence .Th eprincipl ei sbase do nLotka-Vol - terraequation si nwhic hmobilit yi sno texpressed .I timplie stha tever y individualo fa populatio ncompete swit hever yindividua lo fth eothe rpo ­ pulation,whic hmean stha tmobilit yi sunlimited .T otes tth ecompetitiv e

108 Coexistence exclusion principle under thecondition s iti sderive d for, twospecie s were defined identically (both fungivorous grazers)an dhavin g unlimited mobility (they could reach anylocalit y inth eare a ineac h time step). Just aspredicte d byth eprincipl e oneo f them went extinct.Th eproba ­ bility wasfoun d tob eonc e per14 1generations . Insom e computer simu­ lation runson ealread y gotextinc t after some tenso fgenerations .

species A fungivorous grazer intolerant to drought species B fungivorous browser tolerant to drought

• species A fungivorous grazer intolerant to drought species Bfungivorou s browser intolerant to drought

species A fungivorous grazer intolerant to drought species Bfungivorou s browser Intolerantt o drought twice asmobil e asspecie s A

never dry increasing chance ofdrough t

Figure 6.11. a) Log numbers of a fungivorous grazer, intolerant to drought, and a fungivorous browser, tolerant to drought, along a gradient with, from left to right, increasing probabilities of drought, b) Log numbers of a fungivorous grazer and a fungivorous browser, both intolerant to drought, along the same gradient as a. c) Log numbers of a fungivorous grazer and a fungivorous browser, both intolerant to drought, along the same gradient as a. The browser has twice as high a mobility as the grazer.

Mobilityo fspecies ,however ,i sno tunlimite di nreality .Th equestio n iswhethe r theprincipl e alsohold swhe nmobilit y isrestricted . Carrying outth esam e simulationwit hth esam e identically defined speciesbu tno w havinga restricte dmobilit y (randomwal ktyp evalu e10 )decrease dth epro ­ babilityo fextinctio no feithe ron eo fthe mt oonc epe r6 6millio ngene ­ rations.I npractic e thisimplie s infinitecoexistenc ei ncas eo frestric ­ tedmobility . Thus thecompetitiv e exclusion principle doesno tapply .

109 Microarthropod communities

Figure 6.12. The log ratio of numbers of a fungivorous grazer (spl) and an opportunistic herbo-fungivore (sp2) in the presence of a herbivorous grazer during the first ten generations ; individual mobility of the opportunistic herbofungivore varies from 1.1 to 5 times that of each of the grazers.

d

\ 3 \ 1 ~N \ > 2', 3 | !

unsuitable area 1 : ; 2 \ ' : not occupied suitable area 2I area with low density o! / / \ \ !o o !1 ! 2 | 3 |are a with high density

iii ( ' i ii / 3 iii i ' i HI 3 'i

Figure 6.13. Distribution over the grid of seven coexisting species using only two food sources. Per species four areas are distinguished: unsuitable areas (0), suitable but not occupied areas (1), areas with low population densities (2), and areas with high population densities (3). Species definitions (a-g) are given in Table 6.2.

110 Coexistence

Three species systems

Increasing thenumbe r of competing species in themode l leads toa nenor ­ mous increase of potential combinations of species co-occurrences. Only some of the most interesting combinations are summarizedhere . Givena fungivorou sgraze ran da herbivorou sgrazer ,wha tqualitie smus t a third species, feeding onbot h food types,hav e tob e able tosurvive , or even tooutcompet e the two others.Addin g aherbofungivorou s grazer to thetw ograzer sresulte di na slo wbu tstead yincreas eo fth eherbofungivo ­ rousgraze ra tth ecos to fth etw ofoo dspecialists .Whe n insteado fa her ­ bofungivorousgraze ra nopportunisti cherbofungivor e (browser-type)wa sin ­ troduced,whic hconsume smor e foodtha nth egrazers ,th ebrowse rwa s found tob e gradually outcompetedb y the grazers.However ,whe n thebrowse r had agreate rmobilit ythe ni tha dgoo dprobabilitie s tocoexis twit hbot hgra ­ zers. Figure 6.12 showsth e lograti oo fth efungivorou s grazer toth eop ­ portunisticherbofungivor e inth epresenc e ofa herbivorou s grazer.Du et o thedefinitio n of the opportunistic herbofungivore itaffecte dmostl y the fungivorous grazer. Comparison of Figure 6.12 with Figure 6.9, where a fungivorous browser with increasing mobility competed with a fungivorous grazer, shows that already a little higher mobility of the opportunistic herbofungivores over the two species ofgrazer s permitted coexistence.S o ability tous e more types of food canovercom e abigge r need for food per feeding site,whe n it iscombine dwit h an increased mobility. Here again, coexistence ofmor e species than available resources ispossible .

Table 6.2. Traits of seven species competing together for two types of food. Default values are given inTabl e 6.1, reproduction is ineggs.fe ­ male .year

Feeding guild reproduction mobility drought frost heath

a fungivorous grazer default 5 - + + b fungivorous browser default 5 + + + c herbivorous grazer default 5 - + + d herbivorous browser default 5 + + + e herbofungivorous grazer 16 3 + - - f opportunistic herbofungivore default default + - + g fungivorous browser 16 phoretic + + +

111 Microarthropod communities

Multispecies systems

From the above results coexistence seemed possible for more species than thenumbe ro favailabl e resources.Moreover ,whe nmobilit ywa s restricted, specieswit h identicalniche s could coexist,makin g thenumbe r of species in a community theoretically almost equal to the maximum number of individuals. Six feeding guilds have been distinguished and defined so far. In the former sectiondifference s inth eus eo ffoo do r theneede damoun to f food couldb ecompensate d forb yothe r traits.No w inon esimulatio n experiment representatives of all six guildshav ebee nmad e to compete for two types of food: greenplant s (algaeo r organic matter)an d fungi.Tabl e 6.2 pre­ sents the characteristics of these species.Figur e 6.13 presents the dis­ tribution of the species inth e simulated area. Distinctionha sbee nmad e betweenunsuitabl earea s (e.g.th efrequenc yo fdrough t isto ohig hfo rth e drought intolerant species)potentiall y suitable areaswhic har eno toccu ­ pied (due to strong competition), areas with low densities and finally areaswit hhig h densities.I tappeare d still tob en oproble m foron emor e species next to the sixorigina l feeding guild representatives to survive in the model. This species was obligately phoretic and had a rather low overall density;wit h respect to its feedingbehaviou r itbelonge d to the fungivorousbrowsers .Not e thato nal l spots inth e simulated field three ormor e speciescoexist .Bearin g inmin d thatothe r representatives ofth e feeding guilds with roughly similar traits might also survive because of the restricted mobility of almost all species,w e may conclude that this simple model theoretically allows coexistence for more species than available resources.

DISCUSSION

A model as presented here allows simulation of real soil microarthropod speciescompositions .Th eparameter sneede d forthi smode lca nb e obtained relatively easily, assuming independence among parameters (e.g. between reproductionan ddrough tconditions ).B yvaryin gon evariabl ea ta tim eth e sensitivityo fth emode lfo rth eparameter swa sestimated .I tappeare dtha t especially theperio da specie sca nsurviv ewithou tfoo d (Fig.6.10 ) ist o be measured as precisely as possible. However, many more data are needed tosimulat e realspecie scommunitie s andeve nwit hprecisel ymeasure ddat a themode lwil lno tgiv ea realisti cpredictio nabou tcommunit y composition because of the following limitations of themodel .Th e difference between browser and grazer is defined in this model as a difference in need for

112 Coexistence

amounto ffood ,a nassumptio nwhic hca nonl yb e truewhe nbot h speciesar e about equally sized with an about equal metabolic rate,whic h is a sim­ plification ofreality .Anothe r factorno t specified in thismode l is the availability of food. The fact that small species can obtain their food from small cavitieswher e other species cannot reach it (except Pelopidae with specially shaped chelicerae) is not considered. So the step to the fieldstil lwil lb erathe rbig .A compariso nwit hfiel ddat a (Siepel 1992), therefore,i squit eprecariou sdu et oothe rdifference s amongspecie s than use of foodonly .Moreover , thesedifference s inreproduction , generation times, and mobility may oftenb e linked to the use of food. Species com­ prised inth ecategorie s 'fungivorousbrowsers ' and 'fungivorous grazers' mayb ecomparabl ewit hrespec t tothei rlife-histor y inth ementione dstu ­ dy. In (semi-)natural grasslands theproportio no ffungivorou s grazers is muchhighe r than that of fungivorous browsers, aswa s shown inth e model. Allspecie scomprise d in'herbofungivorou sgrazers 'hav emuc h longergene ­ ration times, lower fecundities, and lower mobilities than the average fungivorous browser or grazer, or opportunistic herbofungivores. The choice for thelytoky as the type of reproduction was made both to keep the model simple and clear and the relative importance this type of reproductionha s insoi lmites .Simulatin g sexual reproduction ina mode l based on individuals would give some extra difficulties, such as for example the longevity ofspermatophore s deposited bymales .Thes e sperma- tophores are deposited with andwithou tpresenc e of females,an dar esub ­ jectt oprédatio nan ddestructio nb ymould s (TrâvniCek, 1979).Althoug h it isa simplificatio no f reality the choice for thelytoky instead of sexual reproduction isprobabl yno tessentia l forth eresult so fth esimulations . On the other hand, the model served well the purpose of testing theo­ ries. Itwa s showntha tth emode lsupporte d thespecie sdiversit yhypothe ­ siso fHusto n (1979),bu tth ecompetitiv eexclusio n (Hardin1960 )onl ywhe n mobilitywa sunlimited ,a simplici ti nth eequation so fLotk aan dVolterra . Restrictingmobilit yshowe dtha tcompetitiv eexclusio nfailed .Th eparame ­ tervalu e (1-10)o fmobilit ydi dno tinfluenc eth eoutcom eo fth esimulati ­ onver ymuch .Th e facttha t individualswer e restricted tog oste pb y step throughadjacen t fieldswa sth emos t important.Ste pb y stepmovement s are themos tcommo ni nnatur e inmos tmicroarthropod s andals o inothe r groups of organisms, although the real size of the grid cells with their own independent conditions may be bigger. Thus, the competitive exclusion principle may atbes tb e approached by themos tmobil e species. Inpredator-pre y interactionsth erecognitio no fth eimportanc eo f spa­ tialvariabilit y is quite common. Nachman (1987a,b ) found a stabilizing globaleffec ti nacarin epredator-pre ysystem swit ha characteristi c 'hide- and-seek' pattern, but with local instabilities. Kareiva (1987) stressed the importance of an organisms dispersal behaviour (behavioural response

113 Microarthropod communities to fragmentation) forclaryfyin g theunexpecte d destabilization ofpreda ­ tor-prey interactions in ladybirds and aphids on golden rods. This beha­ vioural response againi si nfac tth emobilit ybetwee npatches .Hassei l et al. (1991)sho wi nmode lsimulation soveral lpersistenc eo fhost san dpara - sitoids ina subdivide denvironmen t inhost-parasitoi d associations.Host s then are aggregated and constant fractions ofbot h hosts and parasltoids maymov et oneighbourin gpatches ,eve nwit hrandoml y searchingparasltiod s and without explicit density-dependency. Atkinson and Shorrocks (1981) pointed earlier to the importance of divided and ephemeral resources for thehig hspecie sdiversit y in Drosophila species,whic ha sa matte ro ffac t meansa restrictio n inmobilit y forth elarvae .Larva ear eno tabl e tomov e from one ephemeral resource to another. In a cage experiment Shorrocks (1991)actuall ydemonstrate d thatth e inferiorcompetito rma ypersis twit h thesuperio rspecie swhe nth espac ei sdivide di nephemera lpatches ,where ­ as the inferior competitor iseliminate d inth e samebu tundivide d space. Both inpredator-pre y interactions,host-parasitoi d associations andcom - petionbetwee nspecies ,mobilit y appears tob eo fgrea t importance forth e persistence of the species indifferen t ways. Nextt oth eimportanc eo fmobilit y themode lha sshow ntha tth eorigina l niche concept (Hutchinson 1957,Schoene r 1989) is too restricted. Itap ­ peared thatspecie sma y compensate theles ssuccessfu lus eo fth esam ere ­ sources thanbette r competitors with non-resource related traits such as thefecundity ,th emaximu m starvationperiod ,an dindividua lmobility .So , thequestio npu tforwar db ysom eauthor s (e.g.Silvertow n1987 )ho ws oman y species can coexist while they are competing for a far lower number of resources is solved on the basis of this work and others (Janzen 1970, Huston 1979,Tilma n 1982). Ingeneral ,coexistenc e may occurwhe n species cannot reach a level of total exploitation of resources either through abiotic factors (e.g.disturbances :Husto n1979 )o rthroug hbioti c factors such aspredator s (Janzen 1970), resource ratios (Tilman 1982), andlife - history compensations of differences inexploitatio n levels (this study). Moreover, coexistence may occur when species have a restricted mobility (this study). Afterall ,w ema ywonde rwh y there ares ofe w species rather thanwh y there are somany .

REFERENCES

Anderson, J.M., 1975. The enigma of soil animal species diversity. In: Vanek,J . (ed.)Progres s insoi lzoology ,Jun kBV ,Th eHagu epp .51-58 . Arthur, W., 1987. The niche in competition and evolution. John Wiley & Sons, Chichester,UK .

114 Coexistence

Atkinson,W.D .& B .Shorrocks ,1981 .Competitio no na divide dan dephemera l resource: a simulation model.Journa l ofAnima l Ecology 50,461-471 . Binns, E.S., 1982. Phoresy as migration - some functional aspects of phoresy inmites .Biologica l Reviews 57,571-620 . Grubb, P.J., 1977. The maintenance of species richness in plant communities. The importance of the regeneration niche. Biological Reviews 52,107-145 . Janzen, D.H., 1970.Herbivore s and thenumbe r of tree species in tropical forests. American Naturalist 104, 501-28. Hardin, G., 1960. The competitive exclusion principle. Science 131, 1292-1297. Hasseil, M.P., H.N. Comins &R.M . May, 1991. Spatial structure and chaos in insect population dynamics.Natur e 353,255-258 . Huston, M., 1979. A general hypothesis of species diversity. American Naturalist 113, 81-101. Hutchinson, G.E., 1957.Concludin g remarks. Cold Spring Harbour Symposia in quantitive biology 22,415-427 . Kareiva,P .,1987 .Habita tfragmentatio nan dth estabilit yo fpredator-pre y interactions. Nature 326,388-390 . Karppinen,E. ,1958 .Übe rdi eOribatide n (Acar.)de r finnischenWaldböden . Annales Zoologica Societas ZoologiesBotanic a Fennics 'Vanamo' 19(1), 1-43. Metz, L.J., 1971.Vertica l movement ofAcarin a under moisture gradients. Pedobiologia 11,262-268 . Moritz,M. , 1965.Untersuchunge n über denEinflu ßvo n Kahlschlagmaßnahmen aufdi eZusammensetzun gva nHornmilbengemeinschafte n (Acari:Oribatei ) norddeutscher Laub- und Kiefernmischwälder. Pedobiologia 5, 65-101. Nachman,G .,1987a .System sanalysi so facarin epredator-pre yinteractions . I. A stochastic simulation model of spatial processes. Journal of Animal Ecology 56,247-265 . Nachman,G .,1987b .System sanalysi so facarin epredator-pre yinteractions . II. The role of spatial processes in system stability. Journal of Animal Ecology 56,267-281 . Schoener, T.W., 1989. 4. The ecological niche. In: Cherrett, J.M. (ed) Ecological concepts: the contribution of ecology to an understanding of the natural world. 385 p. Blackwell,Oxford , 79-113. Shorrocks, B., 1991. Competition on a divided and ephemeral resource: a cageexperiment .Biologica lJourna lo fth eLinnea nSociet y43 ,211-220 . Siepel,H .& C.F .va nd eBund ,1988 .Th e influence ofmanagemen t practices onth emicroarthropo dcommunit yo fgrassland .Pedobiologi a31 ,339-354 . Siepel,H .,1992 .Recoverin go fnatura lprocesse si nabandone dagricultura l areas: decomposition oforgani c matter. In: Zombori,L . & Peregovits, L. (eds) Proc. 4th ECE,Budapest , pp. 374-379. Silvertown, J., 1987. Introduction to plant population ecology. 2nd ed. Longman Scientific & Technical,Harlow , UK. Tilman,D. , 1982.Resourc ecompetitio nan dcommunit y structure.Monograph s inPopulatio n Biology 17,Princeto nUniversit y Press,Princeton , N.J. Trävniöek, M., 1979. Spermatophores of some oribatids of the family Liacaridae (Acarina: Oribatei). Vëstnik Öeskoslovenské SpoleCnosti Zoologické 43,223-239 .

115 Competitive exclusion is not a general ecological principle

Theprincipl e ofcompetitiv e exclusion (Hardin,1960 )i sthough t tob e the most general one in ecology (Arthur, 1987). Of two species occupying the sameniche ,on ewil l outcompete theothe rwhe n resources are limited. The principleseem sa tvarianc ewit hth eoverwhelmin gspecie sdiversity ,parti ­ cularly in plants and invertebrates. Ecologists working on these taxa, thereforepropose dsevera ladditiona lhypothese s thatallo wby-passin gth e principle.Thi swa sdon eeithe rb yweakenin g the impacto fcompetition ,o r bydistinguishin g extranich edimension s toreduc enich eoverlap .Th e crux of the principle,however , isbasicall y formed by the equations of Lotka andVolterr a which implicitly assume unlimited individual mobility. Thatassumptio nma yexplai nth edifferenc eo fopinio nbetwee necologist s adopting the principle (MacArthur & Levins 1967,Piank a 1973,Cod y 1974, Gurnell 1985), often working with mobile vertebrates, such as reptiles, birds, and mammals, and those reluctant to adopt the principle, often working with less mobile invertebrates or plants.Th e latter group, also oftenstrugglin gwit h thenich econcep tan dderive dprinciples ,formulate d new concepts onhig h species diversity on asmal l scalewit h few, limited resources (Silverton 1987,Husto n 1979,Connel l 1971,Janze n 1970,Tilma n 1982, Grubb 1977,Shmid a& Ellne r1984 ,Taylo r& Taylo r 1977,Shorrock s et al. 1984,Warne r & Chesson 1985). Their question is,ho w can many species coexist without outcompeting each other? Several hypotheses by-passing the competitive exclusion principle havebee n formulated toexplai n the observed species diversity. Specieswit h thesam enich ema ycoexis twhe nnon eo fthe mreache s itslimi t inpopulatio n numbers due todisturbance s (Huston 1979). Inhost/pre y ag­ gregates,predator s ordisease sma ypreven t ahost/pre y fromreachin g such high densities and hence from outcompeting other species (Connell 1971, Janzen 1970).Accordin g toth eresource-rati ohypothesi s (Tilman1982 )tw o species can coexist and use the same resources without outcompeting each

117 Microarthropod communities other,becaus eo fdifferin gresourc eexploitatio nefficiency .Juvenile sma y require different resources than adults resulting innich e separation in themor evulnerabl ejuvenil ephas e (Grubb 1977).Accordin g toth eaggrega ­ tionhypothesi s (Shmida & Ellner 1984) intra-specific competition within aggregates ismor e importanttha ninter-specifi c competition,thu sdecrea ­ sing the role of the latter (but see Connell 1971 and Janzen 1970). In insects, competition may be reduced by spatial factors (Taylor & Taylor 1977), especially in ephemeral and discrete resources (Shorrocks et al. 1984). The storage-effect hypothesis (Warner & Chesson 1985) focuses on temporal aspects: competing species can coexist when their recruitment fluctuates asynchronously. Apart from suchhypothese salleviatin g the impacto fcompetition , iti s hypothesized thatman y speciescoexis tbecaus e themobilit yo fth eindivi ­ duals is restricted. A model was constructed for evaluating life-history tactics, feeding guildsan dadaptation s ofcoexistin g soilmite st othei rbiotope s (Chapter 6). The model assumed logistic growth for fungi in each of 15.000grids ; the value ofK of this function did not influence equilibrium population size of fungivorous mites.A s foodwa s limited in supply, competitionoc ­ curred. Two identically defined species were competitors for two sets of runs. Inbot h sets of runs, the species were initially completely mixed. Extinctionoccurre dstochastically .Accordin gt oth eLotka-Volterr amodel , inth efirs t seto frun smobilit ywa sunlimite d forbot h species:al lgri d cells could be reached at each time step by any individual (52 steps per generation). The mean chance of extinction of either species appeared to be once in14 1generations .Thus , forunrestricte d mobility, thecompeti ­ tive exclusionprincipl e indeedheld . Inth e second set ofruns , mobility was limited to adjacent grid cells at each time step. The mean chance of extinctiono feithe r speciesthe nwa sonc e in66.086.71 2generations ,thu s approaching an evolutionary time scale; differences between the two sets ofrun swer e significant (F-test:p<0.001) . Species stillwer e completely mixedan dfoo dwa slimite d (Fig.7.1) .So ,coexistenc ewa s infinitefo rre ­ strictedmobilit yo fth eindividuals ,i.e . thecompetitiv e exclusionprin ­ cipledi dno tapply .Therefor e iti shypothesize d that theles smobil ein ­ dividuals are, the less effective competitive exclusion between species becomes.

Is this model realistic? Thelytokously reproducing species are suffi­ ciently similar totes tth emode la sthei rasexua l reproductionresult s in clone formation, clones differing only to an ecologically irrelevant de­ gree. From the above hypothesis it is to be expected that formation of clones will be rarest in the most mobile species, and commonest in those withrestricte dmobility .Thi si sexactl ywha ti sfound :mos t thelytokously reproducing species are found among plants and invertebrates, and within those groups,the y are the leastmobil e species.Thelytok y ismor e common

118 Competitive exclusion

in flightless weevils and euedaphic springtails than in dragonflies and butterflies, more common in oribatid mites than in obligately phoretic mesostigmatid mites (Suomalainen, 1962,Chapte r2) .

^ "-m-ftfp

B

Figure 7.1. Distribution patterns of species 1 (A), species 2 (B) and food (C) over grid sections after 100 generations. Species were defined as being identical and their mobility was restricted per time-step to orthogonal neighbouring grid cells.

Speciationwil lb e faster inles smobil e than inver y mobile species,th e former lacking competitive exclusion. Stanley (1989)mention s ineffective dispersala sa promotio no fspeciation ,bu tcontinue stha tthi s ineffective dispersal also increases rate of extinction. This last assumption may be questionable now. Thismeans ,therefore ,tha t thebalanc e between specia­ tion and extinction is changed, or that a higher rate of extinction has other causes. Recently, thedistinctio n of localversu s globalmovement s (individual mobility!)als o gave surprising results inparasitoid-hos t relationships: localmovement s stabilized Nicholson-Baileymodel s thatwer eunstabl e per grid cell in arrays larger than 15x 15 (Hassell et al. 1991). Introducingrestricte dmobilit yo findividual sa sa paramete rca nresul t ina genera ltheor yo fcoexistenc ean d localdiversificatio no fclone san d specieso nbot ha necologica lan da nevolutionar y timescale .Thi spossibi ­ lity should, therefore, be tested experimentally, and be formalized in equations on competition and predator-prey relationships.

119 Microarthropod communities

REFERENCES

Arthur, W., 1987. The niche in competition and evolution. John Wiley & Sons,Chichester , UK. Cody, M.L., 1974. Competition and the structure of bird communities. Monographs in population biology 8, Princeton University Press, Princeton, N.J. Connell, J.H., 1971. On the role of natural enemies in preventing competitive exclusion insom emarin e animals andrai n forests.In :De n Boer, P.J. & G.R. Gradwell (eds) Dynamics of populations, PUDOC, Wageningen, The Netherlands. Grubb, P.J., 1977. The maintenance of species richness in plant communities. The importance of the regeneration niche. Biological Reviews 52,107-145 . Gurnell, J., 1985. Woodland rodent communities. In: Flowerdew, J.R., J. Gurnell &J.H.W . Gipps (eds)Th e ecology ofwoodlan d rodents,ban k voles andwoo d mice. Symposia Zoological Society London 55,377-411 . Hardin, G., 1960. The competitive exclusion principle. Science 131, 1292-1297. Hasseil, M.P., H.N. Comins & R.M. May, 1991. Spatial structure and chaos in insect population dynamics. Nature 353,255-258 . Huston, M., 1979. A general hypothesis of species diversity. American Naturalist 113,81-101 . Janzen, D.H., 1970. Herbivores and the number of tree species in tropical forests.America n Naturalist 104,501-28 . MacArthur,R.H .& R .Levins ,1967 .Th elimitin gsimilarity ,convergenc ean d divergence of coexisting species.America n Naturalist 101, 377-385. Pianka, E.R., 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4, 53-74. Shmida, A. & S.P. Ellner, 1984. Coexistence of plants with similar niches. Vegetatio 58,29-55 . Shorrocks,B .,J .Rosewell ,K .Edward s&W.D .Atkinson ,1984 .Interspecifi c competitioni sno ta majo rorganizin gforc ei nman y insectcommunities . Nature 310,310-312 . Silvertown, J., 1987. Introduction to plant population ecology. 2nd ed. Longman Scientific & Technical,Harlow ,UK . Stanley,S.M. , 1989.Fossils ,macroevolution ,an dtheoretica lecology .In : Roughgarden,J .,R.M .Ma y& S.A . Levin (eds)Perspective s inecologica l theory, Princeton University Press,Princeton ,N.J. , 125-134. Suomalainen,E. ,1962 .Significanc e ofparthenogenesi s inth eevolutio no f insects. Annual Review of Entomology 7,349-366 . Taylor, L.R. & R.A.J. Taylor, 1977. Aggregation, migration and population mechanics. Nature 265,415-421 . Tilman, D., 1982. Resource competition and community structure. Monographs in population biology 17, Princeton University Press, Princeton, N.J. Warner, R.R. & P.L. Chesson, 1985. Coexistence mediated by recruitment fluctuations:a fiel d guide toth estorag e effect.America nNaturalis t 125,769-787 .

120 8

General discussion

A BRIEF OVERVIEW OF CURRENT APPROACHES

Themajorit yo fstudie so nsoi lmicroarthropo dcommunitie sar e inspiredb y thehig hnumber smicroarthropod sreac h insoi lan dth e important role they are thought topla y innutrien t cycling and soil fertility {e.g. Badejo & Lasebikan 1988,Hàgva r 1988,Hàgva r& Kjenda l 1981,Fage r 1968,Ibarr a et al. 1965,Lagerlö f& Andre n1988 ,Peterse n& Luxto n1982 ,Seasted t et al. 1989). Themos tsimpl ewa yo fstudyin genvironmenta lan dhuman-induce deffect s on microarthropod communities is to take soil samples, extract the microarthropods, count the numbers, either in total or by systematic groups, and repeat this after the measures to be studied are taken. In better experimental designs also repeatedly sampled unaffected control plotsar e included inth eanalysis .Example s ofsuc hstudie sar eAbo-Kora h et al. 1984, Badejo & Lasebikan 1988, Burghouts et al. 1992, Ehler & Frankie 1979, Gasdorf & Goodnight 1963, Holt 1981, Mallow et al. 1984, Plowman1981a ,b .A commo nfeatur eo fthes estudie s isa lac ko fsystemati c detail. Although sometimes quite forcing reasons for this lack of detail exist, such as insufficient systematic knowledge or time shortage, the results of these studies are of limiteduse . Inman y other community studies soilmicroarthropod s are identified to the species level. Instudie s focussedo n the community levelusuall y the average reaction pattern of soil microarthropods onwhateve r factors are described, taking into account numbers, species diversity and changes in the speciescompositio n (e.g.Abbot t et al. 1980,Aok i 1976,Athias-Binch e 1983,Curr y& Mome n1988 ,Hàgva r& Amundse n1981 ,Kanek o1985 ,Lebru n1965 , Siepel & Van de Bund 1988, Zyromska-Rudzka 1979). Due to the enormous speciesdiversit yo fsoi lmicroarthropod san dth eman ydifferen tway sthes e

121 Microarthropod communities

speciesar eaffecte db yhuma ninfluences ,i ti softe nimpossibl et oextrac t clearpattern s from thisamoun t of information.Moreover , themajorit y of this work is based on correlations and gives no grip on possible causal mechanisms. In studies focussed on the species level in the past decades much information on biotope conditions of particular species has been obtained.Thes e studiescontai nman y faunisticelement san dma yals o serve well in future research for comparison ofbiotop e data per species (e.g. André 1985, 1986, Bukva et al. 1976, Colloff 1983, 1988,Daleniu s 1962, Engelmann1972 ,Fujikaw a1970 ,1975 ,Haarlo v1960 ,Hamme r 1952,HuÇ u1982 , Karg1986 ,Karppine n1955 ,1958 ,Knüll e1957 ,Luxto n1981a ,b ,c ,d ,Märke l 1958, 1964,Met z 1971,Mitchel l 1979,Murph y & Jalil 1963, Norton 1983, Oswald& Mint y1970 ,1971 ,Pand e& Berthe t1975 ,Pop p1970 ,Poursi n& Pong e 1984,Pug h& Kin g1988 ,Rajski 1970 ,Rih a1951 ,Schult e et al. 1975,Stamo u & Sgardelis 1989,Weigman n& Kratz 1981,Woo d 1967a,b) . Usher et al. (1982)stresse d the importance toals o study generalnatu ­ ralhistory ,life-histor ystrategie san decologica lphysiolog yo findividu ­ al species ofmicroarthropods . Examples of such autecological studies are relatively fewi nsoi lmicroarthropod s (e.g. André& Vögtli n1982 ,Athias - Binche 1977,1981 ,1982 ,Binn s 1982,Butche r et al. 1971,Grandjea n1950 , Lions & Gourbière 1988, Madge 1964,Mitchel l 1979, Pan & Shimida 1991, Schulte 1974, Somme 1981, Somme & Conradi-Larssen 1977, Wallwork 1960, Wallwork et al. 1984,Youn g 1980). Thevalu e of these studies liesparti ­ cularly inth efac t thatth especie scharacteristic s measuredma yb evali d on every location, every time the species is found ina sample,whic h may stepb y step explainth eloca lcompositio no fth esoi lmicroarthropo d com­ munities.A commo nfeatur eo fspecies-oriente dcommunit y studies,however , is that they result in much information per species, but little insight into the diversity and coexistence of soil microarthropods. Inthi s thesis species characteristics of soilmicroarthropods , either from literature data or from ownexperiments ,wer e the startingpoin t for explanation of reaction patterns in soil microarthropod communities. The structureo fmicroarthropo dcommunities ,i nbot hnatura lan ddisturbe dbio - topes and during the process of decomposition of organic matter, was elucidated by the classification of life-history tactics,base d on well- defined traits (Chapters 2 & 3). The function of soil microarthropod communitieswa selucidate db yassemblin gmicroarthropod s infeedin gguild s (Chapters 4 & 5). In a simulation model both life-history traits and feeding guilds were connected to investigate whether a relatively low degreeo fefficienc y of foodus ecoul db ecompensate db y arelativel y high degreeo fadaptatio n inlife-histor y traits,thu senablin gmor especie st o coexist than there are resources available (Chapters 6& 7) .

122 General discussion

LIFE-HISTORY TACTICS

A multidimensional classification of twelve life-history tactics was de­ veloped based onwell-define d life-history traits covering reproduction, oviposition,development ,synchronizatio nan ddispersa l (Chapter 2). Forms ofreproductio nwer epreferre di nth eclassificatio nabov ereproductio nra ­ tes. The most wide-spread form, after sexual reproduction, turned out to be thelytoky (asexual reproduction,whereb y females layunfertilize d eggs fromwhic h againfemale shatch) . Inthi styp eo freproductio nn ochang e in geneticcompositio ntake splace ;group so findividual sshar eth esam egeno ­ type ('clones'). Constancy of the environment was hypothesized, and was found, to favour this type ofreproduction . Constant biotopes such asfo ­ restsoils ,an dth elate rstage s inth edecompositio nproces sha d acompa ­ rativelyhig hfractio no fthelytokousl yreproducin gmicroarthropod s (Chap­ ter 3). Constancy of the environment could alsob e createdb yman-induce d pollution. Persistent pollution indeed also led to a high fraction of thelytokously reproducing animals (Chapter 3). Th e basic assumption here is, thatdurin g thefirs tpollutio nal lspecie sar eaffecte d (mostanimal s die), but by chance, in anumbe r of species, some part of the population appears to be resistant. Thelytokously reproducing animals then have an advantage oversexuall yreproducin g ones,becaus ea resistan t femalegive s rise to resistant off-spring. Sexually reproducing species have the dis­ advantage ofpossibl e recombination of the resistant genotype; theresis ­ tant genome is not inherited as such by all off-spring. Besides that, asexually reproducing species generally show a higher rate of increase, because they produce more females. Several forms of synchronization were classified, from overcoming a harshseaso nb ya simpl e slow-downo flife-processes ,t oobligat e diapause with aphysiologica l base (Chapter 2).Ecologicall y these traits could be regardedasadaptation st oirregular ,unpredictabl econdition s (forinstan ­ ceflooding )o non esid e toadaptation s toregular ,predictabl e conditions (for instance seasonality) on the other side.Regula r disturbances ledt o an increase of specieswit hwell-develope d synchronization tactics. E.g., the annual filling up and the gradual draining ofa barrag e resulted ina regular disturbance at theborders ; species at rest during flooding were very abundant (Chapter3) . Traitsfo rdispersa lwer egroupe di ndirectiona lmigratio n (phoresy)an d undirectionalmovement s(anemochory ). Phoreticspecie s(carrier-unspecific ) were very dominant during the first stages of litter decomposition, and irregular unpredictable disturbances also led to an increase of phoretic species, again especially those with obligate carrier-inspecific phoresy (Chapter3 ). Differentatio nshoul db emad ebetwee nobligat ean dfacultativ e

123 Microarthropod communities phoresy andbetwee ncarrier-specifi c andcarrier-inspecifi cphoresy .Con - trarily towha tusuall y isassume d (Binns1982 )phores y appearedno t tob e ar-selecte dtrait .Carrier-specifi cphores y appeared tob eK -o rS-selec - ted rather than r-selected. Incontras t toth emultidimensiona l systemo flife-histor ytactic spre ­ sented in Chapter 2, former classifications of life-history tactics (MacArthur& Wilso n1967 ,Greenslad e1983 ,Grim e1977 ,Hol m1988 ,Southwoo d 1977,Stearn s1976 )di dno tpermi tpractica lus e inapplication s innatur e management orecotoxicology ,becaus e definitions of those strategies were toogeneral ,a tbes tallowin gallocatio no fspecie swit hver ydistinc tlif e histories to strategies (Chapter3) .

FEEDING GUILDS

Fivemajo r feedingguild so fmite swer edistinguished ,base do ngu tcarbo - hydrase activities,i norde r toshe dligh to nth efunctio no fmicroarthro - pods in soil (Chapter4) .

Cumulativemicrobia lrespiratio n (C02production )fro mpulverize dleave s of Avenella (Deschampsia) flexuosa wasmeasure da tregula rinterval sdurin g microcosm experiments. The presence of herbivorous grazers resulted in

neithera nincrease dno ra decrease dC0 2production .Th epresenc eo ffungi - vorous orherbofungivorou s grazers resulted ina n increased production of

C02. Thepresenc eo ffungivorou sbrowser s oropportunisti c herbofungivores

resulted in a decrease of the C02 production. Thus digestion of fungal cell-walls(chitinas eactivity )b yth e(herbo- )fungivorou sgrazer sresulte d in an increased rate of decomposition. Chitin, an important component of the fungal cell-wall,contain s about 7%N . Evidence was obtained that the digestion of fungal cell-walls resulted in the release of extra N, which stimulatedmicrobia lgrowt han drespiratio nan dthu sincrease dth edecompo ­ sitionrat e (Chapter 5). Hence,th etyp eo ffoo ddigestio no fmicroarthro - pods helps to explain their function in soil.

COEXISTENCE

Inchapte r 6an d7 th eaccumulate dknowledg e ofth estructur e and function of soil microarthropod communities was used to shed light on thecoexis ­ tenceo fspecie sb ya mode lincludin gspatia lheterogeneit y offoo dan din ­ cluding mites with different efficiencies of use of food and different life-history tactics. It appeared thatbein g tolerant for short-term en-

124 General discussion vironmental extremes,bein g able tobridg e a long period without food or havinga relativel yhig hmobilit ymigh tcompensat efo ra les sefficien tus e offoo d (digestiono fcell-content sonl y insteado fbot hcell-content san d cell-walls,i.e .browser sversu s grazers). Speciesdiversit ycoul dals ob e highera tlo wfrequencie so fdisturbance, compare d ton odisturbanc ea tal l (exclusiono fth e inferiorcompetitor ),o ra hig h frequencyo fdisturbanc e (neitheron eo fth especie scoul dpersist )i nagreemen twit hth ehypothesi s ofHusto n (1979). Furthermor e itappeare d thatmor e speciestha nresource s could be present without exclusion of one of the competing species. When two species were defined as having the same niche it appeared that when both species had anunlimite dmobilit y either oneo f the specieswen tex ­ tinctwithi n about 140 generations,bu twhe nmobilit y ofbot h specieswa s limited (as it usually is), both species might coexist for more than 66,000,000generation s (Chapter 6). Socompetitiv eexclusio n (Hardin1960 ) may exist onlyb y approximation inver ymobil e species,an d isthu sno t a general ecological principle. In nature two species are never exactly alike,bu t themode l shows that it isno t necessary toassum e thatdiffe ­ rences between species are a prerequisite for their joint existence (Chapter 7). Thepossibl edifferentiatio ni nfoo dchoic e amongsoi lmicro - arthropodsma yb econsiderable ,bu tca nhardl yexplai nthei rspecie sdiver ­ sity. Because the model shows that the lower the mobility in a group of speciesis ,th eles sforcin gi sth eprincipl eo fcompetitiv eexclusion ,th e question 'why are there so many species?' (Anderson 1975) should be re­ placed by 'why are there so few?'.

REFERENCES

Abbott,D.T. ,T.R . Seastedt& D.A .Crossle yjr ,1980 .Abundance ,distribu ­ tion, and effects of clearcutting on Cryptostigmata in the southern Appalachians. Environ. Entomol. 9,618-623 . Abo-Korah,S.M. , M.R.Abo-Elghar ,H .S .A Radwa n& S .E .Salem ,1984 .Vertica l distribution of soilAcar i incotto n fields inMonoufei a governarate, Egypt. Hinufiya J. Agric. 8,431-440 . Anderson, J.M., 1975. The enigma of soil animal species diversity. In: Vanek,J . (ed.)Progres s inSoi lZoology ,Jun kBV ,Th eHagu epp . 51-58. André, H.M. & D.J. Vögtlin, 1982. Some observations on the biology of Camisia carrolli (Acari: Oribatida). Acarologia 23, 81-89. André, H.M., 1985. Associations between corticolous microarthropod communities and epiphytic cover onbark . Hoi. Ecol. 8, 113-119.

125 Microarthropod communities

André,H.M. , 1986.Note s on the ecology of corticolous epiphyte dwellers. 4. Actinedida (especially Tydeidae) and Gamasida (especially Phytoseiidae). Acarologia 27,107-115 . Aoki, J.-I., 1976. Zonation of oribatid mite communities around Sesshogawara ofKusatsu , aspoutin g area of sulphurous acis gas,wit h description of two new species. Bull. Inst. Env. Sei. Techn.Yokoham a A Nat.Univ . 2,177-186 . Athias-Binche, F., 1977. Étude quantitative des uropodides (Acariens: Anactinotriches) d'un arbre mort de la hetraie de la Massane. 1. Caractères généraux dupeuplement . Vie Milieu 27 2C,157-175 . Athias-Binche, F., 1981. Écologie des uropodides édaphiques (Arachnides: Parasitiformes) de trois écosystèmes forestiers. 1. Introduction, material, biologie.Vi e Milieu 31,137-147 . Athias-Binche, F., 1983.Écologi e des uropodides édaphiques (Arachnides: Parasitiformes) de trois écosystèmes forestiers. 6. Similarités interstationnelles. Conclusions générales.Vi e Milieu 33,93-109 . Athias_Binche, F., 1982. Écologie des uropodides édaphiques (Arachnides: Parasitiformes) de trois écosystèmes forestiers. 4. Abondance, biomasse, distributionverticale , steno- et eurytopie.Vi eMilie u32 , 159-170. Badejo, M.A. & B.A. Lasebikan, 1988. Comparative studies of the acarine populations ofa secondar y regrowth forestan da cassav eplantatio n in Ile-Ife, Nigeria. Pedobiologia 32,111-116 . Binns, E.S., 1982. Phoresy as migration - some functional aspects of phoresy inmites .Biol .Rev . 57,571-620 . Bukva, V., M. Daniel & M. Mrciak, 1976. Oribatid mites (Acari, Oribatei) in the nests of small mammals in the western Carpathians. Vest. Ces. Spol. Zool.40 ,241-254 . Burghouts, T., G. Ernsting, G. Korthals & T. de Vries, 1992.Litterfall , leaf litter decomposition and litter invertebrates in primary and selectivelylogge ddipterocar p foresti nSabah ,Malaysia .In :Marshall , A.G. & M.D. Swaine (eds) Tropical rain forest: disturbance and recovery. Proc. R. Soc. Discussion Meeting Sept. 1991,407-416 . Butcher, J.W., R. Snider and R.J. Snider, 1971. Bioecology of edaphic Collembola and Acarina. Ann. Rev. Entom. 16,249-288 . Colloff, M.J., 1983. Oribatid mites associated with marine and maritime lichens on the islandof Great Cumbrae. Glasgow Nat. 20,347-359 . Colloff,M.J. , 1988.Specie s associations oforibati d mites inlichen s on the is land of Ailsa Craig, Firth of Clyde (Acarei:Cryptostigmata) . J. Nat.Hist . 22,1111-1119 . Curry, J.P. & F.M. Momen, 1988. The arthropod fauna of grassland on reclaimed cutaway peat inCentra l Ireland. Pedobiologia 32,99-109 . Dalenius, P., 1962. Studies on the Oribatei (Acari) of the Torneträsk territory in Swedish Lapland. III. The vertical distribution of the moss mites. Kungl. Fys. S. Lund Foerh. 32,105-129 . Ehler,L.E .& G.W .Frankie ,1979 .Arthropo d faunao f liveoa k inurba nan d natural stands inTexas . III.Oribati d mite fauna.J . Kansas Entomol. Soc. 52,344-348 . Engelmann, H.-D., 1972. Die oribatidenfauna des Neissetales bei Ostritz (Oberlausitz). Abh. Ber. Naturk. Mus.Görlit z 47 (5),1-42 . Fager, E.W., 1968. The community of invertebrates in decaying oak wood.

126 General discussion

J.Anim.Ecol. 37,121-142 . Fujikawa, T., 1970. Distribution of soil animals in three forests of NorthernHokkaido .II .Horizonta lan dvertica ldistributio no foribati d mites (Acarina: Cryptostigmata). Appl. Ent. Zool. 5,208-212 . Fujikawa,T. , 1975.Spatia l distribution oforibati d mites insmal l areas II.Th edistributio npatter no fsom eoribati dspecies .Appl .Ent .Zool . 10, 254-262. Gasdorf, E.C. & C.J. Goodnight, 1963. Studies on the ecology of soil arachnids. Ecology 44,261-268 . Grandjean, F., 1950.Observation s éthologiques sur Camisiasegni s (Herrn.) etPlatynothru speltife r (Koch)(Acariens) .Bull .Mus .Natn .Hist .Nat . Paris Ser. 222 ,224-231 . Greenslade, P.J.M., 1983. Adversity selection and the habitat templet. American Naturalist 122,352-365 . Grime,J.P. , 1977.Evidenc e for the existence of threeprimar y strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169-1194. Hardin,G. , 1960.Th e competitive exclusionprinciple . Science 131,1292 - 1297. Haarlov,N. ,1960 .Microarthropod s fromDanis h soils.Ecology , phenology. Oikos 3 suppl, 1-176. Hâgvar, S. & B.R. Kjßndal, 1981. Effects of artificial acid rain on the microarthropod fauna in decomposing birch leaves. Pedobiologia 22, 409-422. Hâgvar, S.& T .Amundsen ,1981 .Effect s oflimin gan dartificia l acid rain on the mite (Acari) fauna inconiferou s forest. Oikos 37,7-20 . Hâgvar,S. ,1988 .Decompositio nstudie si na neasily-constructe dmicrocosm : Effects of microarthropods and varying soil pH. Pedobiologia 31, 293-303. Hammer, M., 1952.Th e oribatid and collembola fauna in some soil samples from Sondre Stromfjord. Entomol.Medd. 26,404-414 . Holt,J.A. ,1981 .Th evertica ldistributio no fcryptostigmati cmites ,soi l organic matter and macroporosity inthre e NorthQueenslan d rainforest soils. Pedobiologia 22,202-209 . Holm, E., 1988. Environmental restraints and life strategies: a habitat templet matrix. Oecologia 75,141-145 . Huston, M., 1979. A general hypothesis of species diversity. American Naturalist 113, 81-101. HuÇu, M., 1982. Strukturelle Eigenschaften von Uropodiden-Zönosen in der Streuschicht verschiedener Waldtypen längs eines Höhengradienten. Pedobiologia 23, 68-89. Ibarra, E.L., J.A. Wallwork &J.G . Rodriguez,1965 .Ecologica l studies of mites found in sheep and cattle pastures. I. Distribution patterns of oribatid mites.Ann . Entomol. Soc. Am. 58,153-159 . Kaneko, N., 1985. A comparison of oribatid mite communities in two different soil types ina coo l temperate forest inJapan . Pedobiologia 28, 255-264. Karg, W., 1986. Vorkommen und Ernährung der Milbencohors Uropodina (Schildkrötchenmilben) sowie ihre Eignung als Indicatoren in Agrarökosystemen. Pedobiologia 29,285-295 . Karppinen, E., 1955. Ecological and transect survey studies on finnish

127 Microarthropod communities

camisiids (Acari,Oribatei) . Ann. Zool. Soc.Vanam o 17 (2),1-80 . Karppinen, E., 1958. Über die Oribatiden (Acar.) der finnischen Waldböden. Ann. Zool. Soc.Vanam o 19, 1-43. Knülle, W., 1957.Di e Verteilung derAcari : Oribatei im Boden. Z.Morph . Ökol. Tiere 46,397-432 . Lagerlöf, J. & 0. Andren, 1988. Abundance and activity of soil mites (Acari) in four cropping systems. Pedobiologia 32,129-145 . Lebrun, P., 1965. Quelques caractéristiques des communautés d'Oribates (Acari:Oribatei )dan s troisbiocénose s deMoyenne-Belgique . Oikos16 , 100-109. Lions, J.C. & F. Gourbière, 1988. Populations adultes et immatures d'Adoristes ovatus (Acarien,Oribate )dan s lesaiguille s de la litière d'Abies alba.Rev . Écol. Biol. Sol 25,343-352 . Luxton, M., 1981a . Studies on the oribatid mites of a Danish beech wood soil. III. Introduction to the field populations. Pedobiologia 21, 301-311. Luxton, M., 1981b . Studies on the oribatid mites of a Danish beech wood soil. V. Vertical distribution. Pedobiologia 21,365-386 . Luxton,M. , 1981c. Studies onth eastigmati c mites of aDanis hbeec hwoo d soil. Pedobiologia 22, 29-38. Luxton,M. ,1981d .Studie so nth eprostigmati cmite so fa Danis hbeec hwoo d soil. Pedobiologia 22,277-303 . MacArthur, R.H. & E.O. Wilson, 1967. The theory of island biogeography. Princeton University Press,Princeton , N.J. Madge,D.S. ,1964 .Th ehumidit y reactions oforibati dmites .Acarologi a 6, 566-591. Märkel, K., 1958 .Übe r die Hornmilben (Oribatei) in der Rohhumusauflage älterer Fichtenbestände des Osterzgebirges. (Eine bodenzoologische Studie auf standortskundlicher Grundlage). Arch.Forstw. 7,459-501 . Märkel, K., 1964. Über die Vertikalgliederung der Oribatiden-fauna in Humusauflagen. Acarologia 6, fasc.h.s. 158-170. Mallow, D., D. Ludwig & D.A. Crossley, 1984. Microarthropod community structure ina coasta l duneecosyste m onJekyl l Island,Georgi a U.S.A. Pedobiologia 27,365-376 . Metz, L.J., 1971.Vertica l movement ofAcarin a under moisture gradients. Pedobiologia 11,262-268 . Mitchell, M., 1979. Effects of physical parameters and food resources on oribatid mites in forest soils.Rec . adv. Acarol.Vo l I.,585-592 . Mitchell, M.J., 1978. Vertical and horizontal distributions of oribatid mites (Acari: Cryptostigmata) in an aspen woodland soil. Ecology 59, 516-525. Murphy,P.W . &M .Jalil ,1963 .Som eobservation so nth egenu sTectocepheus . Acarologia fase. h.s. CRI Cong. Int.Acarol . 1964,187-197 . Norton,R.A. , 1983.Redefinitio n ofMochloribatul a (Acari:Mochlozetidae ) with new species, recombinations, and notes on plant associations. Acarologia 24,449-464 . Oswald, E.T. & L.W. Minty, 1970.Acarin e fauna in southeastern Manitoba: I. Forest soils.Manitob a Ent.4 , 76-87. Oswald, E.T. & L.W. Minty, 1971. Soil acarine fauna of southeastern Manitoba. II.Riparia n communities.Manitob a Ent. 5, 71-78. Pan, C. & K. Shimida, 1991.Col d hardiness of four antarctic terrestrial

128 General discussion

mites in the active season at King George Island. J. Insect Physiol. 37, 325-331. Pande,Y.D .an dP .Berthet ,1975 .Observation so nth evertica l distribution of soilOribatei ina woodlan d soil.Trans .R .Ent .Soc .Lond . 127(3): 259-275. Petersen, H. & M. Luxton, 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 287-388. Plowman, K.P., 1981a. Distribution of Cryptostigmata and Mesostigmata (Acari)withi n the litter and soil layers of two subtropical forests. Austr. J. Ecol. 6, 365-374. Plowman, K.P., 1981b. Inter-relation between environmental factors and Cryptostigmata andMesostigmat a (Acari) in the litter and soil of two australian subtropical forests.J . Anim. Ecol. 50,533-542 . Popp, E., 1970.Communitie s ofmos s mites (Oribatei) ina gradient area. Oikos 21,236-240 . Poursin, J.-M. & J.-F. Ponge, 1984. Étude des peuplements de microarthropodes (InsectesCollembole se tAcarien sOribates )dan stroi s humus forestiers acides de la Forêt d'Orléans (Loiret, France). Pedobiologia 26,403-414 . Pugh, P.J.A. & P.E. King, 1988. Acari of the British supralittoral. J. Natural Hist. 22,107-122 . Rajski, A., 1970. Autecological-zoogeographical analysis of moss mites (Acari, Oribatei) on the basis of fauna in the Poznan environs. Part III. Acta Zool. Cracov. 15,161-257 . Riha, G., 1951. Zur Ökologie der Oribatiden inKalksteinböden . Zool.Jb . Syst. 80,408-450 . Schulte, G., 1974. Brackwasser-Submergenz und latitudinale emergenz küstenbewohnender Milben. Proc. 4th. Int. Congr.Acarol. , 61-67. Schulte,G. ,R . Schuster& H . Schubart,1975 .Zu rVerbreitun gun dÖkologi e derAmeronothride n (Acari,Oribatei )i nterrestrischen , limnischenun d marinenLebensräumen .Veröff .Inst .Meeresforsch .Bremerh .15 ,359-385 . Seastedt,T.R. , M.V.Redd y& S.P . Cline,1989 .Microarthropod s indecayin g wood from temperate coniferous anddeciduou s forests.Pedobiologi a33 , 69-77. Seyd, E.L. &M.R.D . Seaward, 1984.Th e association of oribatidmite s with lichens. Zool.J . Lin. Soc. 80,369-420 . Siepel,H .& C.F .va nd eBund ,1988 .Th e influence ofmanagemen t practices onth emicroarthropo dcommunit yo fgrassland .Pedobiologi a31 ,339-354 . Semme, L.& E.-M Conradi-Larsen, 1977.Cold-hardines s ofcollembolan san d oribatid mites from windswept mountain ridges.Oiko s 29,118-126 . Somme,L .,1981 .Col dtoleranc eo falpine ,arctic ,an dantarcti c Collembola and mites. Cryobiology 18,212-220 . Southwood, T.R.E., 1977.Habitat , the templet for ecological strategies? J. Anim. Ecol.46 ,337-365 . Southwood,T.R.E. ,1988 .Tactics ,strategie s andtemplets .Oiko s52 ,3-18 . Stamou, G.P. & S.P. Sgardelis, 1989. Seasonal distribution patterns of oribatid mites (Acari: Cryptostigmata) in a forest ecosystem. J.Anim.Ecol. 58,893-904 . Stearns, S.C., 1976. Life-history tactics: a review of the ideas.Quart . Rev. Biol. 51,3-47 .

129 Microarthropod communities

Usher, M.B., R.G. Booth & K.E. Sparkes, 1982. A review of progress in understanding the organization of communities of soil arthropods. Pedobiologia 23,126-144 . Wallwork,J.A. ,1960 .Observation s onth ebehaviou ro fsom eoribati dmite s in experimentally-controlled temperature gradients. Proc. Zool. Soc. Lond. 135,619-629 . Wallwork,J.A. , B.W. Kamill &W.G. Whitford, 1984.Lif e styles of desert litter-dwelling microarthropods: a reappraisal based on the reproductivebahaviou r ofcryptostigmati dmites .Suid-Afr .Tydsk .Wet . 80, 163-169. Weigmann, G. & W. Kratz, 1981. Die deutschen Hornmilbenarten und ihre ökologische Characteristik. Zool. Beitr. 27,459-489 . Wood, T.G., 1967.Acar i and Collembola ofmoorlan d soils from Yorkshire, England. I. Description of the sites and their populations. Oikos18 , 102-117. Wood, T.G., 1967.Acar i and Collembola ofmoorlan d soils from Yorkshire, England. II.Vertica l distribution in four grassland soils.Oiko s18 , 137-140. Young, S.R., 1980. Cold hardiness in a temperate cryptostigmatid mite. Oikos 35,350-352 . Zyromska-Rudzka, H., 1979.Disappearanc e of Scutacaridae (Acarina)du e to high concentrations ofminera lnutrient s ina meadow .Pedobiologi a19 , 9-17.

130 Summary

Summary

Resources in soil must be very numerous to explain the species richness with the hypervolume model, in which each species has its own niche, originating from selection for minimal niche-overlap . The objective of this thesis was to investigate whether a limited number of resources can support ahig h number of species. Species of the soil fauna, particular­ lymicroarthropods , were classified according to their life-history tac­ tics and assembled in feeding guilds. In a simulation model the species with different life-history tactics and feeding guillds were included to investigate whether inefficient use of food may be compensated with other traits, such as high mobility, or tolerance for harsh conditions. The simulation model also made it possible to define two species having the same niche and to follow interspecific competition intime .

Microarthropod life-history tactics were based onwell-define d traits in reproduction, oviposition, development, synchronization, and disper­ sal (Chapter 2).I n reproduction more value was given to the type ofre ­ production than to reproductive capacity. Reproduction forms used in the definition of the tactics are: thelytoky, asexual reproduction with fe­ males only, arrhenotoky, asexual reproduction whit males hatching from unfertilized eggs, and sexual reproduction. Also types of oviposition were used as traits: semelparity (all at once) and iteroparity (sprea­ ding in oviposition). The number of developmental stages is rather uni­ form within taxa, differences in rate of development among species with­ in a taxon may be quite large. Within species, the rate of development may be influenced by food quality and temperature. Non-diapause dorman­ cy, a short interruption of development, and real diapause dormancy du­ ring winter or summer are synchronization traits. Semelparity may also be included here as a synchronization trait. Dispersal is usually poorly developed in microarthropods; the walking range is often small. Ways to bridge longer distances are phoresy (hitch-hiking with bigger animals, mostly insects) or anemochory (moving by wind). Twelve life-history tac­ tics were defined, ordered in tactics for synchronization, dispersal,o r different types of reproduction. The classification of tactics was com­ pared with former classifications. Projection of the tactics on MacArthur and Wilson's r-K continuum, the R-C-S triangle of Grime, the time-biotope quadrant of Southwood, and comparison with the classifica­ tion of Stearns, showed that the tactics defined in this thesis are more differentiated. These tactics may be used for other taxa than micro­ arthropods as well; the traits the tactics are based on occur in many groups of organisms.

Allocation of microarthropod species to the life-history tactics was made possible by akey ,whic h made applications innatura l and disturbed or polluted biotopes relatively easy (Chapter 3). Mor e or less natural biotopes, such as the soil of a forest, a grassland, and a salt-marsh, and the process of decomposition of litter, could be characterized quite well in terms of representation by life-history tactics of soil microar­ thropods: in natural biotopes no high fractions of specialized tactics

131 Microarthropod communities were found, but mites with thelytokous reproduction increased in these ­ quence salt marsh - grassland - forest soil, whereas these mites in the later stages in the decomposition process also reached thehighes t frac­ tions. The same good characterization held for disturbed soils: cattle- grazed grasslands had ahig h fraction of phoretic species, theban k of a barrage a high fraction of species with synchronization tactics, and sites with a permanent pollution (persistent pesticides, heavy metals) appeared tohav e high fractions of thelytokously reproducing species.

Feeding guilds were defined on the basis of carbohydrase activities (gut enzymes), particularly cellulase, chitinase, and trehalase (Chapter 4). Cellulase activity points to feeding on plant material, trehalase activity points to feeding on fungal cell-contents , and chitinase acti­ vity indicates that the fungal cell-wall can be digested. Species able to digest cell-contents only are called browsers. Species able to digest cell-walls as well are called grazers. Among the fifty species under study, five large species groups (herbivorous grazers, herbofungivorous grazers, fungivorous grazers, fungivorous browsers, and opportunistic herbo-fungivores) and two single species groups (a herbivorous browser and an omnivore)wer e recognized. The major difference with former clas­ sifications is, apart from the unequivocal definition, the distinction between fungivorous species digesting fungal contents only (browsers), and species digesting both cell-walls and cell-contents (grazers).

In order to examine whether feeding differences would indeed show differences in the decomposition of pulverized leaves, experiments were carried out with representatives of each of the feeding guilds (Chapter 5). In the presence of (herbo)fungivorous grazers ahighe r C02 evolution was measured than in their absence, as expected, while in the presence of fungivorous browsers, or opportunistic herbofungivores, a lower C02 evolution was measured than in their presence. Digestion capacity of the mites indeed appeared tob e important for insight into their function in soil.

In a spatial simulation model the coexistence of the browsers, with their less efficient digestion of food, and the grazers with their more efficient digestion of food, was investigated (Chapter 6 & 7).A higher mobility, or abette r tolerance for short-term environmental extremes, or a longer starvation period of browsers made them coexist with the more efficient users of food. A low frequency of disturbance led to co­ existence of an efficient with an inefficient user of food; not the food but the disturbances limited population size inbot h species in suchca ­ ses. In the simulations a higher number of species was found to able to coexist than the number of resources that were present. Species with identical niches and traits could coexist for about 66 million genera­ tions, as long as their mobility was limited. When both species were defined with unlimited mobility, one of them went extinct in about 140 generations. The simulations, which included the best available know­ ledge on life-history tactics and feeding guilds, indicated that compe­ titive exclusion will rarely occur among soil microarthropods, if at all. Hence, competitive exclusion isno t a general ecological principle.

132 Samenvatting

Samenvatting

Debronne n vanbestaa n ind e bodem zouden zeer talrijk moeten zijn om de bestaande soortenrijkdom teverklare n op grond vanhe t hypervolumemodel, waarin iedere soort eenkarakteristiek e nis bezet en overlap met de nis­ sen van andere soorten door selectie zoveel mogelijk beperkt is. In dit proefschrift wordt onderzocht of het werkelijk nodig is dat elke soort een unieke nis bezet, of dat er met een beperkt aantal bronnen van be­ staan ook sprake kan zijn van grote soortenrijkdom. Een soortenrijke groep van bodemdieren, de microarthropoden, zijn in dit proefschrift ingedeeld in overlevingsstrategieën en voedselgildes. In een simulatie­ model, waarin soorten met verschillende overlevingsstrategieën en ver­ schillende voedselgildes zijn opgenomen,word t onderzocht of een ineffi- ciënter voedselgebruik gecompenseerd kan worden met andere eigenschap­ pen, zoals grotere mobiliteit of tolerantie voor ongunstige periodes. Het simulatiemodel bood ook de mogelijkheid twee soorten met precies dezelfde nis te definiëren en de concurrentie van de soorten door de tijd te volgen. Met behulp van de genoemde indelingen: in overlevings­ strategie, voedselgilde en tolerantie voor ongunstige periodes, konden verschillende aspecten vanhe t leven ind ebode m worden verhelderd.

De overlevingsstrategieën van de microarthropoden zijn gebaseerd op goed gedefinieerde eigenschappen op het vlak van reproduktie, ei-afzet- ting, ontwikkeling, synchronisatie enverbreidin g (Hoofdstuk 2).Wa tbe ­ treft reproduktie is meer waarde gehecht aan de vormen van reproduktie dan aan de reproduktiecapaciteit. Vormen van reproduktie die gebruikt zijn voor de definitie van de overlevingsstrategieën zijn: thelytokie, asexuele reproduktie met alleen vrouwtjes, arrhenotokie, asexuele repro­ duktie met mannetjes uit onbevruchte eieren, en sexuele reproduktie. Ook vormen van erafzet in de tijd: semelpariteit (alles ineens) en iteropa- riteit (spreiding in de tijd) zijn als eigenschappen gebruikt. Aantallen ontwikkelingsstadia van de soorten zijn binnen taxa vrij uniform, maar verschillen in ontwikkelingssnelheid tussen soorten in eenzelfde taxon kunnen groot zijn. Binnen de soort kan de ontwikkelingssnelheid beïn­ vloed worden door voedselkwaliteit en temperatuur. Synchronisatievormen variëren van eenvoudige onderbrekingen van de ontwikkeling tot echte diapausevormen in winter of zomer. Semelpariteit kan ook als synchroni- satievorm worden aangemerkt. Dispersievormen zijn bij microarthropoden vaak slecht ontwikkeld; het loopvermogen is doorgaans gering en de manier om grote afstanden te overbruggen is foresie (het meeliften met grotere dieren, meestal insekten) of anemochorie (windverbreiding). Twaalf overlevingsstrategieën zijn gedefinieerd, gegroepeerd in strate­ gieën gericht op synchronisatie, verbreiding, of verschillende repro- duktievormen. Deze strategieën worden vergeleken met eerdere indelingen. Projectie van de strategieën op het r-K continuum van MacArthur en Wilson, in deR-C- S driehoek van Grime, inhe t tijd-biotoop kwadrant van Southwood, envergelijkin g met de indeling van Stearns, laat zien dat de hier gedefinieerde strategieën beter gedifferentieerd zijn. De strate­ gieën kunnen, behalve bij microarthropoden, ook bij andere levensvormen worden gebruikt; de eigenschappen waarmee ze zijn gedefinieerd komen in allerlei groepenva n organismenvoor .

133 Microarthropod communities

Voor de indeling van soorten microarthropoden in overlevingsstrate­ gieën werd een sleutel ontwikkeld, waardoor toepassing van de indeling in natuurlijke en verontreinigde biotopen betrekkelijk eenvoudig is (Hoofdstuk 3). I n min of meer natuurlijke biotopen, zoals de bodem van eenbos ,ee n grasland en eenkwelder , en gedurende het afbraakproces van bladstrooisel, zijn milieucondities en afbraakstadia goed met de gedefi­ nieerde strategieën te karakteriseren: thelytoke reproduktie heeft een relatief toenemend aandeel ind e reeks kwelder -graslan d -bosbodem ; in de latere stadia van het afbraakproces is thelytoke reproduktie de meest algemene strategie. Voor storingssitutaties blijkt de goede karakterise­ ring ook te gelden: begraasde graslanden hebben een relatief groot aan­ deel foretische soorten, de oeverzone van een stuwmeer heeft een groot aandeel soorten met synchronisatiestrategieën en gebieden met een blij- vende verontreiniging (persistente pesticiden, zware metalen) blijken een groot aandeel soortenme t thelytoke voortplanting teherbergen .

Voedselgildes zijn gedefinieerd op basis van activiteiten van enkele verteringsenzymen uithe t maag-darmkanaal, namelijk cellulase, chitinase en trehalase (Hoofdstuk 4). Cellulase-activiteit duidt op eten van plantaardig materiaal, trehalase-activiteit duidt op eten van schimmel­ celinhouden en chitinase-activiteit geeft aan dat de schimmelcelwand kan worden verteerd. Soorten die alleen celinhouden kunnen verteren worden browsers genoemd. Soorten die ook de celwand kunnenvertere n wordengra ­ zers genoemd. Onderscheiden zijn:herbivor e grazers,herbofungivor e gra­ zers, fungivore grazers, fungivore browsers en opportunistische herbo- fungivoren (elk met verscheidene soorten mosmijten ) en herbivore brow­ sers en Omnivoren (met elk één soort mosmijt uit de vijftig onderzochte soorten). Het belangrijkste verschil met vroeger gebruikte classifica­ ties is de eenduidige definitie enhe t onderscheid tussen soorten die de schimmels slechts ten dele kunnen verteren (browsers) en soorten die de schimmels vrijwel geheel kunnenvertere n (grazers).

Om te onderzoeken of dit laatste onderscheid verschillen te zien zou geven in de afbraak van verpulverd blad door schimmels, zijn met verte­ genwoordigers van elk van de gildes decompositie-experimenten uitgevoerd (Hoofdstuk 5).Zoal s verwacht bleek in aanwezigheid van (herbo)fungivore grazers een grotere microbiële C02-produktie gemeten te worden dan in hun afwezigheid, terwijl in aanwezigheid van fungivore browsers of op­ portunistische herbofungivoren juist een lagere C02-produktie werd ge­ meten dan in hun aanwezigheid. De verteringscapaciteit van schimmel- etende mijtenblijk t dusva n invloed tezijn .

Met behulp van een simulatiemodel werd onderzocht of de minder effi­ ciënte voedselvertering van browsers vergeleken met die van grazers door andere eigenschappen zodanig kan worden gecompenseerd, dat coëxistentie van meer soorten dan bestaansbronnen mogelijk is (Hoofdstukken 6 en7) . Een grotere mobiliteit vanbrowser s kan ze in staat stellen toch inaan ­ wezigheid van de betere voedselconcurrent te overleven, evenals het to­ lereren van korte, onverwachte, ongunstige omstandigheden, ofhe t langer zonder voedsel kunnen. Een lage frequentie van verstoringen blijkt tot coëxistentie van een soort met een inefficiënt voedselgebruik met een

134 Samenvatting soort met een efficiënter voedselgebruik te kunnen leiden; nietvoedsel , maar de verstoringsfrequentie limiteert de populaties in zulke gevallen. Er blijken meer soorten samen voor te kunnen komen dan het aantal gede­ finieerde voedselbronnen. Soorten met een identieke nis en eigenschappen kunnen naast elkaar blijven voortbestaan (gemiddeld 66 miljoen genera­ ties) zolang hun mobiliteit niet onbeperkt is. Geldt voor beide soorten geenbeperkin g inhu n mobiliteit dan sterft eenva n beide soorten binnen gemiddeld 140 generaties uit. Uit de simulaties, gebruik makend van de beschikbare kennis op het gebied van overlevingsstrategieën envoedsel - gildes, blijkt dat uitsluiting door concurrentie bij bodemmicroarthro- poden maar in zeer weinig gevallen een rol zal spelen, als het al zou bestaan. Uitsluiting door concurrentie is dus geen algemeen oecologisch principe.

135 Curriculum vitae

Henk Siepel werd geboren op 31 juli 1959 te Ede. In 1977 behaalde hij het diploma Ongedeeld V.W.O. aan het Christelijk Lyceum te Veenendaal. Daarna studeerde hij biologie aan de Rijksuniversiteit Utrecht, waar hij in 1980 het kandidaatsexamen aflegde. In 1984 studeerde hij af (cum laude) met als hoofdvakken Vegetatiekunde/Botanische Oecologie en Zoologische Oecologie en als bijvak Bodemkunde. Tijdens de doctoraalfase van zijn studie werkte hij als studentassistent bij de vakgroep Zoölogische Oecologie en Taxonomie, de vakgroep Vegetatiekunde en Botanische Oecologie en de vakgroep Petrologie, Mineralogie, Kristallografie, Geochemie en Bodemkunde. In 1984 tradhi j in dienst als toegevoegd onderzoeker bij de vakgroep Zoölogische Oecologie en Taxonomie van de Rijksuniversiteit Utrecht. Eind 1984 kwam hij als onderzoeker evertebraten in dienst bij het toenmalige Rijksinstituut voor Natuurbeheer, nu DLO-Instituut voor Bos- en Natuuronderzoek. In 1993 is hij daar benoemd als projectgroepleider herpetologie, entomologie enmeetnetontwikkelin g ind e afdeling Dierecologie.

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