lable at ScienceDirect

European Journal of Soil Biology 46 (2010) 80e86

Contents lists avai

European Journal of Soil Biology

journal homepage: http: / /www.elsevier .com/locate/ejsobi

Original article

Impact of microarthropod biomass on the composition of the soil faunacommunity and ecosystem processesq

Astrid Rita Taylor a,*, Anne Pflug b, Dagmar Schröter c, Volkmar Wolters d

aDepartment of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, SE-75007 Uppsala, SwedenbNationale Kontaktstelle Lebenswissenschaften, Königswinterer Str. 522-524, DE-53227 Bonn, GermanycUmweltbundesamt GmbH, Environmental Impact Assessment and Climate Change, Spittelauer Lände 5, 1190 Vienna, AustriadDepartment of Animal Ecology, Justus-Liebig-University, Heinrich Buff Ring 26-32 (IFZ), DE-35392 Giessen, Germany

a r t i c l e i n f o

Article history:Received 20 October 2008Received in revised form7 October 2009Accepted 20 November 2009Available online 4 December 2009Handling editor: Hermann Verhoef

Keywords:MicroarthropodsNematodesEnchytraeidsMicrobial biomassMicrocosmTrophic levelInteractionsNitrogen mineralizationCarbon mineralizationLitter mass lossSpruce litter

q The study was carried out at Department of AUniversity, Heinrich Buff Ring 26-32 (IFZ), DE-35392* Corresponding author. Tel.: þ46 18 672216; fax: þ

E-mail address: Astrid.Taylor@ekol.slu.se (A.R. Tay

1164-5563/$ e see front matter � 2009 Elsevier Masdoi:10.1016/j.ejsobi.2009.11.003

a b s t r a c t

The effect of soil organisms on ecosystem processes strongly depends on the composition of the overallcommunity. Community composition however undergoes constant shifts due to pronounced spatio-temporal patterns in biomass and abundance of individual fauna groups. On this background the presentexperiment aimed to assess the potential impacts of shifts in the biomass of a dominant soil fauna group(microarthropods) on total community composition and on ecosystem processes mediated by fauna ormicrobes (e.g. decomposition, nitrogen mineralization).

Microcosms, filled with spruce litter, hosted soil fauna communities that either contained ambientmicroarthropod biomass (control) or two elevated levels of microarthropod biomass (1.5 and 2 foldincrease), while initial microbial biomass and that of other faunal groups remained unaltered. After anincubation period of 2 months, the biomass of microorganisms and fauna groups as well as ecosystemprocess variables were determined.

The increase in microarthropod biomass at the investigated levels induced changes in the faunalcommunity; mainly via negative or positive feeding interactions between microarthropods and theaffected animal groups (Enchytraeidae, Nematoda). The abundance and activity of microorganisms atlower trophic levels however remained unaffected by these alterations; buffering the effect of shifts inthe community structure on ecosystem processes.

� 2009 Elsevier Masson SAS. All rights reserved.

1. Introduction

Decomposition and nutrient cycling in the belowgroundecosystem are regulated by complex abiotic and biotic interactions,in which soil inhabiting organisms play key roles [23]. There isincreasing evidence that the effect of soil organisms on ecosystemprocesses strongly depends on community composition i.e. which(functional) groups are present and at what abundance, rather thanon within group diversity [9]. It is also well established that thebiomass and abundance of different soil fauna groups fluctuatesstrongly in time and space. These spatio-temporal patterns may bea consequence of changes in microclimatic soil properties or due tothe phenological characteristics of the organisms themselves. As

nimal Ecology, Justus-Liebig-Giessen, Germany.46 18 673430.

lor).

son SAS. All rights reserved.

a result community composition undergoes constant shifts in theabundance or biomass of individual fauna groups. These fluctua-tions in community composition are likely to affect ecosystemprocesses not only directly but also indirectly, as changes in one soilfauna group will inevitably induce changes in other groups viaa range of either trophic or non-trophic interactions. In particular,the dominance of functional groups within a community canstrongly depend on interactions like predation and competition butalso on facilitation that affects population dynamics or resourceutilization of single species or groups (e.g. [7] and referencestherein, [46,53]). The combined biotic interactions are of greatimportance in regulating energy flow and nutrient circulationthrough soil communities [48,49]. However, the actual mechanismsof interactions between soil organisms and associated effects onecosystem processes are still poorly understood [3,27].

Numerous studies have investigated interactions withindecomposer communities in one way or another with the majorityaddressing aspects of community diversity or food web complexityin relation to ecosystem functioning (for an overview see [9,37,45]).

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e86 81

These experiments are for the most part designed to either excludedifferent taxonomic or functional groups from the community ormanipulate the complexity of functional groups (group or speciesremoval) (e.g. [18,21,22,24]). Consequently these manipulationsoften result in highly synthetic communities which reduces theapplicability of the results to general conclusions concerning linksbetween community composition and ecosystem processes innatural systems [15].

The aim of the present study was to assess i) how shifts in thebiomass of a dominant soil fauna group (microarthropods) affecttotal community composition with special emphasis on theinvolved faunal interactions and ii) if the induced communitychanges are strong enough to be reflected in fauna- or microbialmediated ecosystem processes (decomposition, nitrogen mineral-ization). To avoid the drawbacks described above we worked withsoil fauna communities whose natural composition in terms ofrelative abundance within and between different fauna groups wasleft as undisturbed as possible. The soil fauna communities werederived by extracting litter material from the L þ FH layer ofa spruce forest. Using a microcosm approach soil fauna communi-ties that contained ambient microarthropod biomass (control)were compared to two communities where microarthropodbiomass had been experimentally increased to simulate spatial ortemporal patterns of community heterogeneity. Strong negativeeffects of increased microarthropod biomass due to food compe-tition were expected on the biomass of enchytraeids andmicrobivorousedetritivorous nematode feeding groups that exploitfood resources similar to those used by the non-predatory micro-arthropod groups. In addition, it was hypothesized that strongergrazing pressure under elevated levels of microarthropod biomasswould also negatively affect microbial biomass [28,13].

2. Materials and methods

2.1. Experimental set-up

The experiment was carried out in 24 microcosms, each con-sisting of an opaque polyethylene-tube (height: 23 cm; diameter:4.5 cm; volume: 723 cm3) with a gauze bottom through whichleachate was collected. The tubes were continuously aerated andthe evolution of carbon dioxide (CO2) was monitored by automaticgas chromatography (Shimadzu GC-14 B). Throughout the 59 daysof the experiment, the microcosms were kept in a climatic chamberunder conditions of constant temperature (13 �C) and permanentdarkness. The water content of the microcosms was maintained at200% dry mass (DM).

Microcosms were filled with litter collected from the O-horizonof a Norway spruce monoculture (Picea abies [L.] Karst.), situated inthe Vogelsberg area (Hesse, Germany; 50�310N, 9�170E) at anelevation between 695 and 730 m a.s.l. (see Taylor et al. [43] forfurther information). After collection, the spruce litter was carefullymixed, and larger twigs, spruce cones, moss, seedlings, etc. wereremoved. This litter hosted the ambient faunal community witha natural level of microarthropod biomass. One portion of this litterwas retained and used to fill the microcosms of the control treat-ment. The remaining litter (standard litter) was used to create twoadditional levels of microarthropod biomass by inoculating it withadditional microarthropods using a high-gradient extractor [52].Microarthropods (collembolans and mites) were extracted fromeither two dry mass equivalents (treatment 1 ¼ T1) or three drymass equivalents (treatment 2¼ T2) of litter from the experimentalsite into one dry mass equivalent of the standard litter. For theextraction procedure that lasted 15 days, the litter used as micro-arthropod source was placed in sampling containers in the topcompartment of the high-gradient extractor and the standard litter

was put into collecting vessels in the lower compartment. Betweenboth compartments, a temperature gradient was created by slowlyincreasing the temperature in the top compartment to a maximumof 30 �C (increase of the temperature within 7 days from 20 �C to30 �C, 8 days at 30 �C) while keeping the temperature in the lowercompartment around 12 �C (water cooling). In order to expose alllitter used in the experiment to similar initial conditions, the litterused to fill themicrocosms of the control treatment was also kept inthe lower compartment of the extractor for 15 days but withoutbeing inoculated. All litter was periodically moistened during theextraction procedure.

For each microarthropod biomass treatment (control, T1, T2), 8replicate microcosms (diameter 4.5 cm) were filled to a height of17 cm (corresponding to a volume of 270 ml) with litter containingthe respectivemicroarthropod biomass level. The initial drymass ofthe litter in eachmicrocosmwas determined from a subsample (seebelow). Additionally, a portion of litter used to fill in each micro-cosm was retained for determination of the initial microarthropodbiomass in the three treatments. Microarthropods were extractedfrom these subsamples (ca. 5 g DM) into ethylene glycol in a high-gradient extractor over a period of 14 days. Microarthropods werethen transferred into 70% alcohol and determined.

2.2. Analytical procedures

At the end of the experiment, the microcosms were destruc-tively sampled. Immediately after sampling, the contents of eachmicrocosm were weighed, carefully mixed and stored in sealedplastic bags at 4 �C. Animal extraction, microbiological and physico-chemical measurements were initiated within 3 days.

Subsamples of 5 g litter were dried at 105 �C for 24 h to deter-mine the water content of the litter material (expressed as litter drymass [%DM]). Mass loss in eachmicrocosmwas then calculated as %mass loss of initial mass. Microbial carbon (Cmic) was measuredwith the fumigation-extraction method [54] assuming a kEC-valueof 2.22 [54]. The amount of K2SO4 (0.5 M) extractable mineral N(Nextr) was determined photometrically from the unfumigatedextracts of the FE-method (PERSTORPANALYTICAL GmbH, Perstorp,Sweden).

2.3. Animal extraction and biomass calculations

Microarthropods were extracted from 4 g dry mass subsamplesfollowing the extraction procedure described above. All collembo-lans were identified to species level using the keys cited by Chauvatet al. [8]. Species known to consume significant amounts of foodtypes other than fungi were either lacking or rare so that collem-bolans were pooled in a single group. Extracted mites were dividedinto the suborders prostigmatic mites, astigmatic mites, meso-stigmatic mites and oribatid mites following Krantz [20]. Adultoribatid mites (except Brachychthoniidae) were identified tospecies level using the keys cited by Taylor and Wolters [42]. Themesostigmatic mites were further divided into the cohorts Gama-sina and Uropodina [20]. Adults and nymphs of the mesostigmaticcohort Gamasina were denoted ‘predatory mites’ and the remain-ing mites were divided into oribatid mites (only adults) and ‘othermites’; with both groups assumed to have mainly fungivorousfeeding habits. The ‘other mites’ consisted of the mite subordersProstigmata and Astigmata, the mesostigmatic cohort Uropodinaand the undetermined nymphal stages of all mite groups (exceptthose of the Gamasina, see above). Nematodes and Enchytraeidswere extracted from additional subsamples (ca. 4 g DM) witha modified O'Connor-wet-funnel-extraction [30]; for the nema-todes extraction was followed by milk-filter cleaning [33]. Enchy-traeids were counted live after extraction, but no further

Table 1Summary of a 2-way ANOVA on the biomass [mg C g�1 DM] of the manipulatedmicroarthropod groups derived from spruce litter samples in a laboratory micro-cosm experiment. The two main effects used in the model were microarthropodbiomass (MB) treatment (3 levels of increasing microarthropod biomass) andsampling time (start, end of experiment). F-values and P-values of main effects andinteractions on each of the dependent variables are presented, n ¼ 40.

MB-treatment [MB] Time [T] MB � T

Microarthropods 17.97***a 15.9*** 1.6 n.s.Collembolans 2.4 n.s. 3.1 n.s. 0.0 n.s.Mites 39.3*** 27.9*** 5.3**Predatory mites 30.1*** 88.9*** 8.9***Other mites 5.5** 16.4*** 0.9 n.s.Oribatid mites 33.1*** 2.7 n.s. 2.1 n.s.

a Significance level of F-value: P < 0.001***; <0.01**; <0.05*; >0.05 ¼ n.s.(not significant).

0

20

40

60

80

100

120

Control T1 T2 Control T1 T2

]M

D1- g

Cgµ[

ssamoiB

Collembolans Predatory mites

0

20

40

60

80

100

120

Control T1 T2 Control T1 T2

gC

gµ[ssa

moiB1-

]M

D

Oribatid mites Other mites

(SD = 52.9)

Fig. 1. Mean biomass [mg C g�1 DM] (SD) of manipulated microarthropod groups inspruce litter monitored at the start (white bars) and the end (black bars) of a laboratorymicrocosm experiment. In contrast to the control, the treatments T1 and T2 weremanipulated to contain elevated microarthropod biomass levels at the start of theexperiment [n ¼ 6 (for control, n ¼ 8)].

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e8682

determination was undertaken. Nematodes were counted, fixed inFormaldehyde, determined to genus level, and classified intofeeding groups [55].

The estimation of microarthropod biomass carbon requires theestimation of microarthropod dry weight based on length/weightregressions for collembolans and length/width/weight regressionsfor mites (see below). The body length of the individual collem-bolan species was estimated using the mean length of each speciesgiven in the determination keys (cf. [8]). Thesemeans were used forcalculating the body dry weight by means of the regression equa-tions given by Tanaka [41] and Petersen [32]. For species notmentioned in these publications, dry weight values of species witha similar body shape were used. Biomass C of collembolans wascalculated using an average C content of 47.5% dry weight [6].Furthermore, age structure was taken into account by assuming theshare of juveniles to be 60% [32], with the body length of juvenilesbeing half that of the respective adults.

In contrast to the collembolans, calculation of oribatid biomasswas based on own measurements on average body length andwidth (abundant species: at least 10 specimens per species; rarespecies: all available individuals). For all other mite groups, sizeclasses were established and for each size class an average lengthand width was determined based on the measurements of at least10 specimens. Average liveweight of mites was calculated using theregression equations and their corrections from Persson and Lohm[31]. The ratio between dry and live weight of all mite groups wasassumed to be 0.4 [31]. Biomass Cwas calculated using an average Ccontent of 47.7% dry weight for all mite groups [6].

Enchytraeid biomass was calculated from abundance valuesassuming an average biomass of 22.152 mg C per individual [6,31].Adult nematodes were distinguished from juveniles and biomassestimates was made from genus-specific abundances according tothe transformation factors provided by Berg et al. [6] and Ekschmittet al. [12].

2.4. Statistical analyses

The impact of the factors ‘microarthropod biomass’ and ‘time’on the manipulated fauna groups was analyzed using 2-wayANOVAs with the biomass of total microarthropods, oribatid mites(adults), predatory mites, ‘other mites’ and collembolans asdependent variables. The response of all other parameters (non-manipulated faunal groups, microbial biomass, functional vari-ables) to the factor ‘microarthropod biomass’ was examined bymeans of 1-way ANOVA using the data measured at the end of theexperiment. Homogeneity of variances was tested using the Lev-ene's-test; normality of residuals was checked visually and usingthe ShapiroeWilk's W test to ensure that the assumptions of theANOVA were met. When necessary, data were normalized prior tostatistical analysis; biomass data and litter variables were logtransformed (log(x þ 1)), percentage data (mass loss [% initial DM])were transformed using arcsine square root. Significant differencesbetween means were determined by computing the Tukey honestsignificant difference test (Tukey HSD test, P < 0.05). All statisticalanalyses were done with STATISTICA� software, version 6.

3. Results

Significant effects of the factors ‘microarthropod biomass’ and‘time’ indicate that the experimental treatments persistentlyaltered total microarthropod biomass (Table 1). At the start of theexperiment, microarthropod manipulation had succeeded ingradually enlarging initial microarthropod biomass from100 � 48 mg C g�1 DM in the control microcosms to 161 �48 mg C g�1 DM in T1 and to 202� 48 mg C g�1 DM in T2. Differences

between the control and the manipulated treatments were signif-icant and were mainly accounted for by a significantly higherbiomass of mites in T1 and T2 (Tukey HSD test, P < 0.05). Thebiomass of collembolans was unaltered (Fig. 1).

At the end of the experiment, totalmicroarthropod biomass inT1and T2 was still significantly higher than in the control (Tukey HSDtest, P < 0.05; microarthropod biomass [mg C g�1 DM] in the threetreatments: control ¼ 160 � 48; T1 ¼ 290 � 65; T2 ¼ 237 � 66).

During the course of the experiment, biomass of predatorymites and ‘other mites’ increased in all treatments (Fig. 1), resultingin a significant effect of time (Table 1). No significant effect of timewas found for collembolans (Table 1), although there was a cleartrend in all treatments for increased biomass (Fig. 1). In contrast tothese three groups, oribatid mites showed a slight tendency todecline over the experimental period (Fig. 1).

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e86 83

The temporal changes in the biomass of predatory mites and‘other mites’ were most evident in T1 (Fig. 1). For the predatorymites, an increase in biomass over timewas significantly negativelycorrelated to their initial biomass in the three treatments (Pearsonproductemoment correlation, r ¼ �0.71, P < 0.001); the ratio offinal to initial biomass decreased from 2.7 in the control to 2.3 in T1and 1.4 in T2. These patterns of community dynamics resulted ina significant treatment � time interaction term (Table 1). For allother microarthropod groups, the effects of the two main factors,microarthropod biomass treatment and time were independent(Table 1).

At the beginning of the experiment, microbial biomass C (Cmic)and the biomass of the unmanipulated fauna groups e nematodesand enchytraeids e were similar between the three biomasstreatments (Tukey HSD test, P < 0.05). Averaged over the threetreatments, nematode biomass was 2.1 � 2.7 mg C g�1 DM andenchytraeid biomass was 418 � 144 mg C g�1 DM (see Fig. 2).Average microbial biomass was 7.3 � 3.0 mg C g�1 DM.

Enchytraeids

0

200

400

600

800

1000

1200

1400

1600

Control T 1 T 2

g C gµ[ ssa

moiB1-

]M

D

0

1

2

3

4

5

6

7

8

9

Control T 1 T 2

g C gµ[ ssa

moiB1-

]M

D

RestBacterivoresOmnivores

Nematodes

Fig. 2. Mean biomass [mg C g�1 DM] (SD) of unmanipulated fauna groups in sprucelitter monitored at the end of a laboratory microcosm experiment. The broken lineindicates mean nematode biomass at the start of the experiment, averaged over thethree treatments. In contrast to the control, the treatments T1 and T2 were manipu-lated to contain higher than ambient microarthropod biomass levels at the start of theexperiment [n ¼ 6 (for control, n ¼ 8)].

Manipulation of microarthropod biomass significantly affectedthe values of nematode and enchytraeid biomass (Table 2). Theeffects on the groups contrasted each other; nematodes (inparticular bacterivores and omnivores) responded positively whileenchytraeids responded negatively to increased microarthropodbiomass (Fig. 2). The response of both groups was particularlystrong in T1.

Biomass treatments did not affect microbial biomass (Cmic) andcarbon turnover (CO2 release, mass loss), but significantly alterednitrogen availability (Table 3, Nextr values [mg g�1 DM] at the end ofthe experiment: control ¼ 71.1 � 9.5; T1 ¼ 90.3 � 7.8; T2 ¼74.1 � 6.3).

4. Discussion

4.1. Effects of elevated microarthropod biomasson other soil organisms

The reduced enchytraeid community growth in microcosmswith elevated microarthropod biomass could be due to bothincreased competition for food and predation. Enchytraeids areconsidered to be 80% fungivorous and 20% general saprophagousfeeders ([11] and references therein). Competition for fungalresources between enchytraeids and the largely fungivorousmicroarthropods could, therefore, have been a significant factorregulating the development of enchytraeid communities. Thisproposal is supported from earlier studies which found competitiveinteractions with fungivorous microarthropods to be a strongregulative force on enchytraeid communities (e.g. [50]). Huhta et al.[16], also using a microcosm approach, only observed a negativeeffect of microarthropods on enchytraeids when a mixed (preda-tory and microbivorous) community was present, but not whenonly predatory mites were added. This would suggest that the mainmode of influence of microarthropods on enchytraeids was throughcompetition for food and not direct predation.

The initial biomass ratio of fungivorous microarthropods toenchytraeids in the different treatments appears to have beenimportant in determining the interactions between the two groups.A ratio of 1:6 at the start of the experiment may have been suffi-cient for a competitive advantage for the enchytraeids in thecontrol, whereas a lower ratio of ca. 1:3 in the manipulated

Table 2Summary of a 2-way ANOVA on the biomass [mg C g�1 DM] of microorganisms andunmanipulated fauna groups derived from spruce litter samples in a laboratorymicrocosm experiment. The two main effects used in the model were micro-arthropod biomass (MB) treatment (3 levels of increasing microarthropod biomass)and sampling time (start, end of experiment). F-values and P-values of main effectsand interactions on each of the dependent variables are presented, n ¼ 40.

MB-treatment [MB] Time [T] MB � T

MicroorganismsMicrobial carbon (Cmic) 0.1 n.s.a 11.2** 0.2 n.s.

MicrofaunaNematodes 6.0** 13.3*** 0.2 n.s.Fungivores 2.5 n.s. 10.2 n.s. 2.0 n.s.Bacterivores 5.0* 3.2 n.s. 0.1 n.s.Omnivores 6.6** 34.0*** 1.0 n.s.Root feeders 2.3 n.s. 1.5 n.s. 0.0 n.s.Predators 0.6 n.s. 4.7* 0.6 n.s.

MesofaunaEnchytraeids 3.3*b 29.2*** 0.7 n.s.

a Significance level of F-value: P < 0.001***; <0.01**; <0.05*; >0.05 ¼ n.s. (notsignificant).

b P ¼ 0.051.

Table 3Summary of a 1-way ANOVA on functional parameters derived from spruce littersamples at the end of a laboratory microcosm experiment. The main effect used inthe model was microarthropod biomass treatment (3 different levels of micro-arthropod biomass), n ¼ 20.

MB-treatment

Functional parametersNextr [mg g�1 DM] 8.3**a

CO2 [mg C] 0.1 n.s.Mass loss 1.2 n.s.

a Significance level of F-value: P < 0.001***; <0.01**; <0.05*; >0.05 ¼ n.s. (notsignificant).

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e8684

treatments may have altered the balance between the two groupsin favour of microarthropods.

Most experiments investigating nematodeemicroarthropodinteractions focus on the presence/absence effect of micro-arthropods at field densities. Commonly, in these experimentssignificantly lower numbers of nematodes are reported in thepresence of microarthropods compared to the treatment wheremicroarthropods are absent [16,17,43]. In contrast to this in thepresent study, nematode biomass increased in the manipulatedbiomass treatments. In particular, bacterivorous and omnivorousnematodes seemed to have benefited from elevated levels ofmicroarthropod biomass. It seems evident that this can be attrib-uted to their dietary advantage of utilizing a different food sourcerange than the mainly fungivorous microarthropods. Many nema-todes have similar generation times to their food sources and areable to respond rapidly to changes in microbial populations [2].Community dynamics of nematode feeding groups can thereforereflect fungal and bacterial biomass production [40].

Microbivorous soil fauna can directly affect the microbialbiomass pool by grazing on both bacteria (predominantly protozoa,bacterivorous nematodes) and fungi (mainly fungivorous nema-todes, microarthropods, enchytraeids) (e.g. [35]). Litter comminu-tion by soil fauna is often assumed to enhance microbial activityand, therefore, decomposition in general [14]. However, indecomposer communities it is not unusual that changes in abun-dance at higher trophic levels do not reflect down to the lowesttrophic level and, similar to the present experiment, a range ofstudies have not been able to show effects of mesofauna grazing onmicrobial biomass or activity [44]. Potential reasons for the overallvery variable response of microorganisms to grazing have beendiscussed extensively in the literature (see [26]). In general, theinaccessibility of microorganisms, particularly fungi, within litterdebris and compensatory growth by microorganisms as a responseto grazing, can result in an apparent weak impact of soil inverte-brates on microbial biomass.

4.2. Effects of induced structural changes in the faunal communityupon functional parameters

In the absence of plant uptake and exogenous N inputs, theprocesses regulating mineral N levels in the type of microcosms asused in the present experiment are primarily N mineralization,N immobilization bymicroorganisms, leakage fromdamaged fungalhyphae due tomesofauna grazing and faunal excretion of mineral N[1,4]. The latter phenomenon is an important feature of fungivorousand bacterivorous soil animals which, due to low assimilation effi-ciency, excrete a considerable proportion of assimilated N as faecalmatter [10]. A stimulatory effect of these organisms on N minerali-zation has been reported from a number of studies (e.g. [35,38,43]).In the present study, the significantly higher Nextr values in T1compared to the control and T2 at the end of the experiment lendsupport to the reported positive influence of microarthropods upon

Nextr. However, this apparent relationship is an artefact of the initialdifferences in Nextr among the three treatments; T1 had slightlyelevated levels of Nextr at the start of the experiment (control:43.8 mg g�1 DM; T1: 51.9 mg g�1 DM; T2: 36.5 mg g�1 DM), and thisdifference was maintained until the end of the experiment. Themean increases inNextr over the course of the experiment, in each ofthe treatments, were essentially identical (Tukey HSD test, P< 0.05;control: 36.3 mg g�1 DM; T1: 37.4 mg g�1 DM; T2: 37.6 mg g�1 DM),demonstrating that changes in microarthropod biomass had littleimpact upon Nextr.

The experiment demonstrated that litter mass loss, used as anindicator of decomposition, was not affected by the structuralchanges in the decomposer community. Decomposition studiesusually report an initial rapid loss of littermass due to the leaching ofsoluble litter materials followed by a slower rate of decompositionwhich is thenprimarily the result of biotic processes [36]. Litter of thepresent study can be expected to have reached this latter decompo-sition stage as it was collected from the litter layer of a forest soil andnot collected fresh from the tree. A low decomposition rate togetherwith the short exposure period could explain the low mass loss,which could have masked differences between the treatments.However, inmoderately decomposed litter, the impact of mesofaunaon decomposition has found to be negligible compared to that of themicroorganisms [5,51]. Therefore, it is more likely that mass lossmostly reflected the lack of treatment effect on microbial biomass.

4.3. Temporal development of microarthropod groupsin the different biomass treatments

In all three biomass treatments, 95% of the adult oribatid miteindividuals belonged to only three species (Tectocepheus velatus,Chamobates borealis, Suctobelbella subtrigona; unpublished results).These three species all have generation times in excess of the two-month experimental period [25]. The long generation time of thisgroup of microarthropods could therefore explain why no increasein oribatid mite biomass was observed over the course of theexperiment. A significant impact of predation on communitydevelopment is unlikely as most adult oribatid mites are heavilysclerotised (see [29]); among the fungivorous microarthropods inthe microcosms, oribatid mites were the fauna group the leastlikely to be affected by mite predators.

Predatory mites generally prefer soft-bodied soil fauna speciesor stages andmany predominantly feed on collembolans [19]. Closepredatoreprey associations between mesostigmatic mites andcollembolans have been found in both microcosm studies and fieldinvestigations [17,34]. Therefore it was somewhat surprising thatno effect of predation was observed for Collembola in the presentstudy; in contrast, collembolan biomass was stable. An explanationcould be that reproduction compensated for predation. Themajority of collembolan species found in this study are capable ofparthenogenetic reproduction and have short generation times[39]. These attributes could have counteracted an effect by preda-tors, even over the relatively short experimental period.

The generally short developmental times of mesostigmaticmites [19] allow a rapid response to changes in prey density. Thebiomass treatments in the present study effectively increasedpotential prey items in all microcosms. However, there was a clearnegative relationship between the relative increase in predatorymite biomass and the initial microarthropod biomass. Despitevarying degrees of specialisation on specific prey groups (e.g.collembolans), most predacious mite species are general predators,which include feeding on other predatory mites. This so-called‘intra-guild predation’ can be sufficiently intense to severely reducethe community of predators [47]. It is possible that increasednumbers of predatory mites in T1 and T2 intensified intra-guild

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e86 85

predation, resulting in the observed pattern of community devel-opment of predatory mites.

5. Conclusions

The present experiment provided evidence that microarthropodbiomass is a driving factor steering the biomass of other soil faunagroups. An effect of microarthropods is mainly brought about viaindirect negative and positive interactions rather than constitutinga direct impact resulting from predation. In contrast to the initialhypothesis, an increase in microarthropod biomass and therebyinduced changes on other soil fauna groups had little effect uponthe microbial community and the functional parameters Nextr andmass loss.

From an ecosystem perspective the results indicate that shortterm spatial or temporal fluctuations in the biomass of some majorcomponents of the soil fauna community seem to be buffered bythe soil system and do not reflect down on the microbial commu-nity and ecosystem process level. In the present study a moderateincrease in microarthropod biomass was investigated, it remainsunclear if and to what extend the effect of a reduction in micro-arthropod biomass would also be buffered by the system.

Acknowledgements

The authors would like to thank M. Kröckel, M. Leonardt andC. Tandler for their help during the experimental set-up, samplecollection and treatment. The authors are grateful to A.F.S. Taylorfor valuable comments and linguistic revision. The study wascarried out within the context of the GLOBIS project (Global Changeand Biodiversity in Soils) funded by the EU.

References

[1] J.D. Aber, J.M. Melillo, Terrestrial Ecosystems, second ed. Harcourt/AcademicPress, San Diego, CA, 2001.

[2] J.M. Anderson, Spatiotemporal effects of invertebrates on soil processes. Biol.Fertil. Soils 6 (1988) 216e227.

[3] M.H. Beare, D.C. Coleman, D.A. Crossley Jr., P.F. Hendrix, E.P. Odum,A hierarchicalapproach to evaluating the significance of soil biodiversity to biogeochemicalcycling. in: H.P. Collins, G.P. Robertson, M.J. Klug (Eds.), The Significance andRegulation of Soil Biodiversity. Kluwer, Dordrecht, 1995, pp. 5e22.

[4] G. Benckiser, Fauna in Soil Ecosystems Recycling Processes, Nutrient Fluxesand Agricultural Production. Marcel Dekker, New York, 2001.

[5] B. Berg, U. Lohm, H. Lundquist, A. Wirén, Influence of soil animals ondecomposition of Scots pine needle litter. in: T. Persson (Ed.), Structure andFunction of Northern Coniferous Forests e an Ecosystem Study, Ecol. Bull. 32(1980) 401e409.

[6] M.P. Berg, J.P. Kniese, J.J.M. Bedaux, H.A. Verhoef, Dynamics and stratificationof functional groups of micro- and mesoarthropods in the organic layer ofa Scots pine forest. Biol. Fertil. Soils 26 (1998) 268e284.

[7] M. Bonkowski, W. Cheng, B.S. Griffiths, J. Alphei, S. Scheu, Microbialefaunalinteractions in the rhizosphere and effects on plant growth. Eur. J. Soil Biol. 36(2000) 135e147.

[8] M. Chauvat, A.S. Zaitsev, V. Wolters, Successional changes of Collembola andsoil microbiota during forest rotation. Oecologia 137 (2003) 269e276.

[9] D.C. Coleman, From pets to paradoxes: linkages between soil biota and theirinfluences on ecological processes. Soil Biol. Biochem. 40 (2008) 271e289.

[10] D.C. Coleman, P.F. Hendrix, Invertebrates as Webmasters in Ecosystems. CABIPublishing, Wallingford, 2000.

[11] W.A.M. Didden, Ecology of terrestrial Enchytraeidae. Pedobiologia 37 (1993)2e29.

[12] K. Ekschmitt, G. Bakonyi, M. Bongers, T. Bongers, S. Boström, H. Dogan,A. Harrison, A. Kallimanis, P. Nagy, A.G. O'Donnel, B. Sohlenius, G.P. Stamou,V. Wolters, Effects of the nematofauna on microbial energy and mattertransformation rates in European grassland soils. Plant Soil 212 (1999) 45e61.

[13] A.H. Fitter, I.R. Sanders, Interactions with the soil fauna. in: M.F. Allen (Ed.),Mycorrhizal Functioning. Chapman and Hall, London, 1992, pp. 333e354.

[14] K. Hedlund, M. Sjögren Öhrn, Tritrophic interactions in a soil communityenhances decomposition rates. Oikos 88 (2000) 585e591.

[15] D.U. Hooper, F.S. Chapin III, J.J. Ewel, A. Hector, P. Inchausti, S. Lavorel,J.H. Lawton, D.M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setälä, A.J. Symstad, J. Vandermeer, D.A. Wardle, Effects of biodiversity on ecosystemfunctioning: a consensus of current knowledge. Ecol. Monogr. 75 (2005) 3e35.

[16] V. Huhta, P. Sulkava, K. Viberg, Interactions between enchytraeid (Cognettiasphagnetorum), microarthropod and nematode populations in forest soil atdifferent moistures. Appl. Soil Ecol.(1e3) (1998) 53e58 (special issue).

[17] R. Hyvönen, T. Persson, Effects of fungivorous and predatory arthropods onnematodes and tardigrades in microcosms with coniferous forest soil. Biol.Fertil. Soils 21 (1996) 121e127.

[18] S. Kaneda, N. Kaneko, Collembolans feeding on soil affect carbon and nitrogenmineralization by their influence on microbial and nematode activities. Biol.Fertil. Soils 44 (2008) 435e442.

[19] W. Karg, Acari (Acarina), Milben Parasitiformes (Anactinochaeta), CohorsGamasina Leach, Raubmilben, second ed. Tierwelt Deutschland, Teil 59 GustavFischer Verlag, Jena, 1993.

[20] G.W. Krantz, A Manual for Acarology, second ed. Oregon Stage University,Corvallis, 1978.

[21] J. Laakso, H. Setälä, Sensitivity of primary production to changes in thearchitecture of belowground food webs. Oikos 87 (1999) 57e64.

[22] J. Laakso, H. Setälä, A. Palojärvi, Influence of decomposer food web structureand nitrogen availability on plant growth. Plant Soil 225 (2000) 153e165.

[23] P. Lavelle, D. Bignell, M. Austen, P. Giller, V. Behan-Pelletier, V. Garey,P. Hawkins, G. Brown, M. St John, W. Hunt, E. Paul, Vulnerability of ecosystemsat different scales: role of biodiversity and implications for management. in:D. Wall (Ed.), Sustaining Biodiversity and Functioning in Soils and Sediments.Island Press, New York, 2004, pp. 213e224.

[24] M. Liiri, H. Setälä, J. Haimi, T. Pennanen, H. Fritze, Soil processes are notinfluenced by the functional complexity of soil decomposer food webs underdisturbance. Soil Biol. Biochem. 34 (2002) 1009e1020.

[25] M. Luxton, Studies on the oribatid mites of a Danish beech wood soil e IV.Developmental biology. Pedobiologia 21 (1981) 312e340.

[26] J. Mikola, H. Setälä, No evidence of trophic cascades in an experimentalmicrobial-based soil food-web. Ecology 79 (1998) 153e164.

[27] J. Mikola, R.D. Bardgett, K. Hedlund, Biodiversity, ecosystem functioning andsoil decomposer food webs. in: M. Loreau, S. Naeem, P. Inchausti (Eds.),Biodiversity and Ecosystem Functioning: Synthesis and Perspectives. OxfordUniversity Press, Oxford, 2002, pp. 169e180.

[28] K. Newell, Interactions between two decomposer Basidomycetes anda collembolan under Sitka spruce: distribution, abundance and selectivegrazing. Soil Biol. Biochem. 16 (1984) 235e239.

[29] R.A. Norton, Evolutionary aspects of oribatid mite life histories and conse-quences for the origin of theAstigmata. in:M. Houck (Ed.),Mites: Ecological andEvolutionary Analyses of Life-History Patterns. Chapman and Hall, New York,1994, pp. 99e135.

[30] F.B. O'Connor, Extraction of enchytraeid worms from a coniferous forest soil.Nature 175 (1955) 815e816.

[31] T. Persson, U. Lohm, Energetical significance of the Annelids and arthropods ina Swedish grassland soil. Ecol. Bull. 23 (1977) 1e211.

[32] H. Petersen, Estimation of dry weight, fresh weight, and calorific content ofvarious Collembolan species. Pedobiologia 15 (1975) 222e243.

[33] J.J. s'Jacobs, J. Van Bezooijen, A Manual for Practical Work in Nematology.Wageningen Agricultural University, The Netherlands, 1984.

[34] S. Scheu, D. Albers, J. Alphei, R. Buryn, U. Klages, S. Migge, C. Platner,J.-A. Salamon, The soil fauna community in pure and mixed stands of beechand spruce of different age: trophic structure and structuring forces. Oikos 101(2003) 225e238.

[35] D. Schröter, V. Wolters, P.C. De Ruiter, C and N mineralisation in the decom-poser food webs of a European forest transect. Oikos 102 (2003) 294e308.

[36] T.R. Seastedt, D.A. Crossley Jr., V. Meentemeyer, J.B. Waide, A two-year study ofleaf litter decomposition as related to macroclimatic factors and micro-arthropod abundance in the southern Appalachians. Holarctic Ecol. 6 (1983)11e16.

[37] H. Setälä, Sensitivity of ecosystem functioning to changes in trophic structure,functional group composition and species diversity in belowground foodwebs. Ecol. Res. 17 (2002) 207e215.

[38] H. Setälä, E. Martikainen, M. Tyynismaa, V. Huhta, Effects of soil fauna onleaching of nitrogen and phosphorus from experimental systems simulatingconiferous forest floor. Biol. Fertil. Soils 10 (1990) 170e177.

[39] H. Siepel, Applications of microarthropod life-history tactics in naturemanagement and ecotoxicology. Biol. Fertil. Soils 19 (1995) 75e83.

[40] B. Sohlenius, S. Boström, Effects of climate change on soil factors and meta-zoan microfauna (nematodes, tardigrades and rotifers) in a Swedish tundrasoil - a transplantation experiment. Appl. Soil Ecol. 12 (1999) 113e128.

[41] M. Tanaka, Ecological studies on communities of soil Collembola in Mt. Sobo,southwest Japan. Jpn. J. Ecol. 20 (1970) 102e110.

[42] A.R. Taylor, V. Wolters, Responses of oribatid mite communities to summerdrought: the influence of litter type and quality. Soil Biol. Biochem. 37 (2005)2117e2130.

[43] A.R. Taylor, D. Schroeter, A. Pflug, V. Wolters, Response of different decomposercommunities to the manipulation of moisture availability: potential effects ofchanging precipitation patterns. Glob. Change Biol. 10 (2004) 1314e1324.

[44] B. Vedder, C. Kampichler, G. Bachmann, A. Bruckner, E. Kandeler, Impact offauna complexity on microbial biomass and N turnover in field mesocosmsfrom spruce forest soil. Biol. Fertil. Soils 22 (1996) 22e30.

[45] D.H. Wall, A.H. Fitter, E.A. Paul, Developing new perspectives from advances insoil biodiversity research. in: R.D. Bardgett, M.B. Usher, D.W. Hopkins (Eds.),Biological Diversity and Function in Soils. Cambridge University Press, Cam-bridge, 2005, pp. 3e27.

A.R. Taylor et al. / European Journal of Soil Biology 46 (2010) 80e8686

[46] D.H. Wall, J.C. Moore, Interactions underground: soil biodiversity, mutualism,and ecosystem processes. BioScience 49 (1999) 109e117.

[47] D.E. Walter, H.C. Proctor, Mites: Ecology, Evolution and Behaviour. CABIPublishing, Wallingford, 1999.

[48] D.A. Wardle, P. Lavelle, Linkages between soil biota, plant litter qualityand decomposition. in: G. Cadisch, K.E. Giller (Eds.), Driven by Nature:Plant Litter Quality and Decomposition. CABI Publishing, Wallingford,1997, pp. 107e124.

[49] D.A. Wardle, G.W. Yeates, The dual importance of competition and predationas regulatory forces in terrestrial ecosystems, evidence from decomposer foodwebs. Oecologia 93 (1993) 303e306.

[50] M.Y. Way, N.E.A. Scopes, Studies on the persistence and effect on soil fauna ofsome soil-applied systemic insecticides. Ann. Appl. Biol. 62 (1968) 199e221.

[51] D.H. Wise, M. Schaefer, Decomposition of leaf litter in a mull beech forest ecomparison between canopy and herbaceous species. Pedobiologia 38 (1994)269e288.

[52] V. Wolters, Ökologische Untersuchungen an Collembolen eines Buchenwaldesauf Kalk. Pedobiologia 25 (1983) 73e85.

[53] V. Wolters, Soil invertebrates - effects on nutrient turnover and soil structuree a review. Z. Pflanzenern. Bodenk. 154 (1991) 389e402.

[54] J. Wu, R.G. Joergensen, B. Pommerening, R. Chaussod, P.C. Brookes, Measure-ment of soil microbial biomass C by fumigation-extraction e an automatedprocedure. Soil Biol. Biochem. 22 (1990) 1167e1169.

[55] G.W. Yeates, T. Bongers, R.G.M. de Goede, D.W. Freckman, S.S. Georgieva,Feeding habits in soil nematode families and genera e an outline for soilecologists. J. Nematol. 25 (1993) 315e331.