Applied Soil Ecology 17 (2001) 19–30

Manipulations of a microbial based soil food web at two arctic sites— evidence of species redundancy among the nematode fauna?

Liliane Ruessa,∗, Inger K. Schmidtb, Anders Michelsenb, Sven Jonassonba Institut für Biologie II, RWTH Aachen, Kopernikusstr. 16, 52056 Aachen, Germany

b Botanical Institute, University of Copenhagen,Øster Farimagsgade 2 D, 1353 Copenhagen K, Denmark

Received 21 March 2000; received in revised form 10 November 2000; accepted 13 November 2000

Abstract

Nutrient limitation is a major factor influencing ecosystem processes in arctic soils, but knowledge on the decomposerfood web interactions and their effects on nutrient cycling is scarce. Manipulations of the soil food web were carried out attwo contrasting subarctic sites, a low altitude heath and a high altitude fellfield. The amount of nutrients and energy in thesoil was increased by NPK fertilization and addition of labile carbon (sugar). Additionally, two bactericides (penicillin andstreptomycin) and a fungicide (benomyl) were applied to manipulate the bacterial and fungal biomass. Experiments werecarried out in a factorial design with repeated additions over four growing seasons.

The present study investigates the effects of the manipulations on the composition of the nematode fauna. It focuses ondiversity and trophic structure and their relationships with soil processes. The application of bactericides had no effect on thenematode fauna, probably due to a high adsorption or low persistence of the antibiotics in the soil, as indicated by a comparablelack of response of target organisms (i.e. bacteria). Generally, the other manipulations caused a shift in dominance structurewith an increase in general opportunists and a decrease inK-strategists. This was reflected in a reduction of the maturityindex. Similarly, species number, richness and diversity declined, and those effects were most pronounced in treatments withthe fungicide benomyl, which was revealed to be a strong toxin to non-target organisms. In contrast to the distinct changesin species structure, the trophic structure was only moderately affected by the manipulations. Relating these findings to theestimates of functional properties at the sites (e.g. microbial biomass, plant growth) indicates considerable redundancy amongthe nematode fauna. The impact of the perturbations on the nematode populations was most severe at the climatically harshhigh altitude fellfield, probably as a result of the lower initial biodiversity (i.e. redundancy) at that site. © 2001 ElsevierScience B.V. All rights reserved.

Keywords:Nematodes; Diversity; Trophic structure; Fertilization; Antibiotics; Benomyl

1. Introduction

Detrital food webs are complex in structure, and thenumber of trophic links may be much higher than inabove-ground food webs (Coleman, 1996). Many in-vestigations focus on the trophic interactions, i.e. the

∗ Corresponding author. Present address: Otto-Hahn-Str. 45,89584 Ehingen, Germany.

feeding relationships between members of differenttrophic levels in a food chain. Recently, the impor-tance of interactions between species within a trophiclevel was addressed (Setälä et al., 1998), indicatingthat ecosystem functioning may be sensitive not onlyto the presence or absence of whole functional groups(e.g. bacterial or fungal feeders), but also to changeswithin these groups (e.g. altered diversity). Nematodeswith their wide feeding range include most functional

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20 L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30

trophic groups present in below-ground food webs.According to the concept of functional redundancy,decomposition models generally regard their influ-ence as dependent on trophic group biomass, not onspecies composition (Ettema, 1998). More changesin primary production are expected by manipulatingentire trophic groups, than single species within agroup.

As in other ecosystems, the species composition,diversity, number and activity of arctic soil nematodesare influenced by complex interactions of climate, soilcharacteristics, plant productivity, and biomass and ac-tivity of microorganisms. A characteristic feature ofarctic soils is their low nutrient supply rate (Nadelhof-fer et al., 1992; Jonasson et al., 1999), but there arefew studies on the decomposer food web interactionsand their effects on nutrient cycling (Ekschmitt et al.,1999; Ruess et al., 1999a; Sohlenius and Boström,1999; Schmidt et al., 2000). Microorganisms in suchsoils may act as a sink or a source for nutrients, as theynot only supply them to plants by mineralization, butmay also decrease their amounts in soil during peri-ods of high microbial demand (Jonasson et al., 1996;Michelsen et al., 1999).

Considering the huge carbon stocks in tundra soils,and the risk of accelerated decomposition and C emis-sion caused by global warming (Nadelhoffer et al.,1992), there is a strong need for a better understand-ing of feeding interactions. In our experiments wemanipulated the decomposer food web of a subarc-tic heath and a high altitude fellfield in two differentways. Firstly, we increased the influx of nutrients andenergy by NPK fertilization or addition of labile car-bon, to minimize the resource limitations for plants,soil microbes and fauna. Secondly, we attempted toalter the microbial community composition by appli-cation of two bactericides or a fungicide. Treatmentswere added repeatedly in a factorial design over fourgrowing seasons and were expected to change thefungal to bacterial ratio, the trophic interactions be-tween microbes and fauna, and the nutrient mineral-ization and availability in the soil. In the present study,species and trophic diversity of nematodes were an-alyzed. Thereby, both the horizontal (within trophicgroup interactions) and the vertical (trophic interac-tions) changes in the food web architecture were as-sessed and related to ecosystem processes. This mayprovide insight into the functional group approach and

into the degree of species redundancy within nema-tode populations.

2. Materials and methods

2.1. Study sites

The study was carried out in August 1996 at twocontrasting sites near Abisko, northern Swedish Lap-land (68◦20′N, 20◦51′E). One site is a subalpine heathwith a species rich dwarf shrub community domi-nated byVaccinium uliginosum(L.) and situated at thetree line at 450 m a.s.l. close to Mount Paddustieva.The other is a high altitude fellfield with a sparsevegetation of dwarf shrubs, mosses and lichens at1150 m a.s.l. on Mount Slåttatjåkka. The climate ofthe Abisko region is subarctic, with a growing sea-son from mid-June until early September. The annualprecipitation in 1996 was 278 mm and the annual airtemperature was−0.5◦C. During the growing seasonin 1996, when the investigations were performed, themean air temperature was 10.2◦C at the heath. Themean soil temperature at a depth of 2 cm (fellfield)and 5 cm (heath) was 6.5 and 7.5◦C, respectively.

At both sites, the bedrock consists mainly ofbase-rich mica schists. The soil at the heath site is agelic gleysol with a well-developed, 10–15 cm deephumus layer. The soil type of the fellfield is a gelicregosol (ramark) with a discontinuous humus layerrarely exceeding 2 cm. Soil pH (in H2O) was 7.1 in0–10 cm depth at the heath site and 5.2 within theupper 0–2 cm at the fellfield. Water content (in % ofDM) measured at sampling date was 237% (0–3 cm)and 197% (3–6 cm) at the heath, and 233% (0–2 cm)at the fellfield. Soil organic matter, determined asloss on ignition (in % of DM), was 82% at the heathand 53% at the fellfield. For more details on climate,vegetation and soil see Jonasson et al. (1996) andMichelsen et al. (1999).

2.2. Experimental design

The experiment was performed in a randomizedblock design. Six blocks containing eight square plots(1 m × 1 m) received the following additions: carbon(250 g/m2 sucrose), fungicide (4 g/m2 Benlate, con-taining 50% of the active component benomyl), and a

L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30 21

mixed NPK fertilizer (5:1.25:3.75 g/m2, respectively)consisting of NH4NO3, NaH2PO4 and KCl. Manipula-tions were performed in a factorial design to give sevendifferent combinations of additions and a control thatreceived no additions, each with six replicates. Thestudy started in spring 1993 with applications in midto late June, just after snowmelt, and again at the endof July. In June 1994, the experiment was extended bytwo additional treatments: bactericide (2 g/m2 strepto-mycin and 2 g/m2 penicillin) and a combined bacteri-cide plus fungicide treatment (six replicates each).

All additions were applied as water solutions(2 l/m2), except for carbon, which was applied asfinely granulated sucrose. Manipulations were per-formed twice every year until the sampling in August1996, where applications were made on 27th Juneand 18th July at the heath site and on 28th June and20th July at the fellfield.

2.3. Nematodes

Sampling took place on 20th (heath) and 22nd (fell-field) August 1996, i.e. after four growing seasons(three for the bactericide and combined bactericideplus fungicide treatments) with environmental ma-nipulations. Soil samples were taken with a soil corer(∅ 2.5 cm) from each treatment plot, at 0–3 and3–6 cm depths at the heath, and 0–2 cm depth (theentire depth of the humus layer) at the fellfield. Ne-matodes were extracted using a modified Baermannmethod (for details see Ruess, 1995a). After 24 h ofextraction at room temperature (10–12◦C) a heatingregime was applied using electric bulbs placed overthe extraction funnels. The temperature in the extrac-tion chamber increased gradually and reached 32◦Cafter 6 h. The extracted nematodes were preserved in4% cold formaldehyde solution. The nematodes ex-tracted were counted (a total of 163 861 individuals)and at least 10% of the individuals of each sample (i.e.a total of 21 600 individuals) were identified to specieslevel.

2.4. Data analysis

Several indices of nematode community structurewere applied. Species richness (according to Yeatesand Bird, 1994) with SR= (s − 1)/loge N andShannon–Wiener diversity index (Pielou, 1971) with

H ′ = − ∑pi loge pi were calculated, wherepi is

the proportion of individuals in theith species,s isthe number of species andN is the number of indi-viduals identified in each sample. Nematode specieswere assigned to feeding groups according to Yeateset al. (1993). The trophic diversity was calculated asT = 1/

∑p2

i , wherepi is the proportion of individ-uals in theith trophic group (Freckman and Ettema,1993).

The maturity index (MI) proposed by Bongers(1990) for non-plant parasitic nematodes was used,with MI = ∑

vipi , wherevi is the c − p value ofthe ith taxon andpi is the proportion of theith taxon.Colonizers (c) and persisters (p) are extremes on ascale from 1 to 5, respectively. The plant parasiteindex (PPI; Bongers, 1990) for plant parasitic speciesand the

∑MI (Yeates, 1994) including all species

were determined in a similar manner.Treatment effects on dominance and trophic struc-

ture were tested by ANOVA with block, carbon,fertilizer and fungicide applications as main effects,including all interactions. Interactions between blockand other main effects were excluded from the mod-els. Degrees of freedom were five for block and onefor each of the main effects and the interactions.Because the treatments with bactericides and com-bined bactericides plus fungicide were initiated 1 yearlater, they were not included in the ANOVAs. Insteadthey were tested using Dunnett’s two tailedt-test fordifferences from the control.

3. Results

3.1. Species diversity

The mean numbers of species observed in the vari-ous treatments at the heath ranged from 16 to 29 and21 to 30 at 0–3 and 3–6 cm soil depths, respectively(Table 1). The occurrence of species was strongly af-fected by the treatments containing the fungicide beno-myl (B). In the 0–3 cm soil layer benomyl resulted insignificantly lower species numbers (main effects fortotal numbers, omnivores, bacterial and fungal feederswith P < 0.001, 0.05, 0.01 and 0.01, respectively),the effect being most evident in the combined BCFtreatment, where the decrease was almost 50% (Tukey,P < 0.05 for total numbers). At 3–6 cm depth the

22 L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30

Table 1Mean numbers of nematode species of different trophic groups observed at the low altitude heath and the high altitude fellfield in differentsoil layersa

K F C C + F B B + F B + C B + C + F SP SP+ B ANOVA

Heath 0–3 cmBacterial feeders 18 16 17 14 13 11 12 11 17 11∗∗∗ B∗∗Fungal feeders 4 4 4 3 3 2 3 2 3 3 B∗∗Plant feeders 5 4 5 4 4 4 4 3 4 4 F∗∗Obligate plant parasites 1 0 1 1 0 1 1 0 1 1Predators 1 1 1 1 1 0 1 0 1 0Omnivores 2 ac 3 a 3 ac 1 ac 1 ac 1 ac 0 b 1 bc 3 1 B∗Total 29 b 27 ab 29 b 23 ab 20 ab 18 ab 19 ab 16 a 28 18∗∗∗ B∗∗∗

Heath 3–6 cmBacterial feeders 16 ab 17 a 13 ab 15 ab 13 b 14 ab 14 ab 13 ab 14 14 B∗∗Fungal feeders 3 4 3 3 4 3 3 3 3 3 B× F∗Plant feeders 4 4 3 4 4 3 4 4 4 4Obligate plant parasites 1 1 1 1 1 1 1 1 1 1Predators 0 1 1 1 1 1 1 1 0 1Omnivores 2 ab 4 a 3 ab 1 b 1 b 2 ab 1 b 1 b 2 1 C∗, B∗∗∗, C × F∗∗Total 25 ab 30 a 24 b 23 b 21 b 22 b 23 b 21 b 24 24 C∗, B∗∗∗, C × F∗,

B × C∗

Fellfield 0–2 cmBacterial feeders 11 a 6 b 9 ac 6 bc 6 bc 4 b 5 b 3 b 10 8 F∗∗∗, B∗∗∗Fungal feeders 2 2 1 2 1 2 1 2 2 2 F∗, Blo∗Plant feeders 4 4 3 3 4 3 3 3 4 4Obligate plant parasites 1 0 1 1 1 1 1 1 1 1Predators 1 a 0 b 0 b 0 b 0 b 0 b 0 b 0 b 1 0∗Omnivores 3 a 1 bc 1 c 0 b 1 bc 0 b 1 bc 0 b 2 1∗∗∗ F∗∗∗, B∗∗∗, B × F∗∗∗,

B × C∗Total 20 a 12 bc 15 b 12 bc 12 bc 8 c 10 bc 9 c 18 15∗ F∗∗∗, C∗, B∗∗∗,

C × F∗, B × F∗a Treatments are: K: control; F: fertilizer; C: carbon; B: benomyl; SP: streptomycin+ penicillin. Results of ANOVAs with significant

effects of the main factors fertilizer (F), carbon (C), benomyl (B) and interactions, Blo: block effect. Multiple comparisons of meansaccording to Tukey (P < 0.05), data with the same or no letters are not significantly different. SP and SP+B are compared to the controlsby Dunnett’s test, but are not included in the ANOVAs.

∗ P < 0.05.∗∗ P < 0.01.∗∗∗ P < 0.001.

negative influence of benomyl was still present withmain effects on total numbers, omnivores and bac-terial feeders being highly significant (P < 0.001,0.001 and 0.01, respectively). More species were ob-served in plots treated with fertilizer only, comparedto plots treated with carbon, benomyl or its combina-tions (Tukey,P < 0.05).

At the fellfield the mean numbers of species ob-served ranged between 8 and 20 (Table 1). All treat-ments, except the bactericide, resulted in significantdeclines in numbers, most evidently so with the app-lications containing benomyl (Tukey,P < 0.05, for

main effects of F, B, C see Table 1). Similarly, to theheath soil, bacterial feeders and omnivores were themost affected.

Species richness (SR) in the 0–3 cm layer at theheath was greatest in the control plots with a valueof 5.84 (Table 2). The strongest reduction in speciesnumbers was found for all benomyl treatments (P <

0.001), but distinct negative main effects were also ap-parent after fertilizer addition (P < 0.05). At 3–6 cmdepth richness ranged between 4.19 and 5.63. A sig-nificant decrease in plots with benomyl (P < 0.01)still occurred. Species diversity (H′) was also strongly

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negatively affected by benomyl (P < 0.01) and fertil-ization (P < 0.001) in the upper soil horizon, whereasin deeper layers the changes were less pronounced andonly significant for benomyl (P < 0.05).

At the fellfield, species richness was highest in thecontrol plots (4.03) and was distinctly reduced in alltreated plots (P < 0.001 and 0.05 for F, B and C,C×F, respectively; Table 2). The decrease was great-est in the BCF plots with a richness value of only 1.70.The diversity of species (H′) showed a similar pattern(P < 0.001 for F, B), but the decline in the manipu-lated soils was less.

3.2. Dominance structure

Table 3 presents the dominance (proportion in per-centage) of the 10 most frequent nematode genera atthe heath and the fellfield. The dominance structurewas strongly influenced by the treatments. At 0–3 cmsoil depth in the heath the following significant maineffects occurred: fertilization had a positive impacton Acrobeloides, and negative onPrismatolaimusand Teratocephalus; effects of benomyl were posi-tive for Acrobeloides, and negative forEudorylaimus,Plectus, Prismatolaimusand Tylencholaimus; appli-cation of carbon affectedAphelenchoidespositively.The bacterial feederCervidellus and the two plantfeedersFilenchusand Malenchusshowed no signif-icant response to the treatments. In the 3–6 cm soillayer, significant treatment effects were still presentbut were generally less pronounced, in particularthose of fertilization. A decrease after bactericideapplication compared to controls (P < 0.05) was ob-served forTeratocephalus, whereas an increase wasfound for Tylencholaimus. As in the upper soil hori-zon, Cervidellus, FilenchusandMalenchuswere notaffected by the manipulations.

At the fellfield the dominance structure alsochanged significantly due to the different treatments.A main positive effect of fertilizer and carbon wasobserved forAphelenchoides. Eudorylaimusshoweda negative response to all manipulations, except to theapplication of bactericide. A main negative fertilizereffect occurred also forMonhystrella, Prismatolaimusand Prodesmora. Additionally, benomyl affectedPlectus, Prodesmoraand Teratocephalusnegatively.As at the heath, the most frequent plant feeders (hereFilenchusandLelenchus) showed no distinct changes.

In the upper soil layer of the heath and the fell-field both the maturity index (MI) and

∑MI were

highest in the control and the bactericide treatedplots (Table 2). The other manipulations reduced MIand

∑MI in the order F > C > B at the heath

(P < 0.001 and 0.01 for B and F, C, respectively)and C > F > B at the fellfield heath (P < 0.001and 0.01 for F and B, respectively). The combina-tion of fungicide and nutrient enrichment treatments(CF, BF, BCF) showed the lowest maturity indices,indicating the highest disturbance. At 3–6 cm depthin the heath, the effects on MI and

∑MI were

less pronounced and most apparent for benomyl(P < 0.05 and 0.001, for MI and

∑MI, respec-

tively) and its combinations, in particular BCF. Theplant parasite index (PPI) ranged between 2.00–2.11and was not affected by the treatments at eithersite.

3.3. Trophic structure

Bacterial feeders were the dominant trophic groupin all plots of the heath site and made up 47–66% ofthe total population (Fig. 1). They were followed byplant and fungal feeders with averages of 20 and 17%,respectively. Obligate plant parasites, predators andomnivores were scarce with less than 6%. The trophicstructure was only slightly affected by the treatmentsand no significant differences were detected, except anegative main effect of fertilizer (P < 0.01) on fungalfeeders at 3–6 cm depth. However, at 0–3 cm depthsome general trends were observed. The proportionof omnivores decreased in all plots treated with beno-myl. Further, in the BCF treated plots a shift from abacterial to a more fungal feeder dominated nema-tode population occurred. In the 3–6 cm layer, effectsof the manipulations were even less pronounced but,as in the upper soil layer, omnivores declined withbenomyl addition.

In the control plots of the fellfield soil, bacterialfeeders (61%) dominated, followed by plant feeders(18%), omnivores (10%) and fungal feeders (9%). Ob-ligate plant parasites (1.3%) and predators (0.7%) werescarce (Fig. 1). The manipulations affected mainlythe ratio of bacterial to fungal feeders, as fertilizationdecreased the proportion of bacterial feeders but in-creased the proportion of fungal feeders significantly(P < 0.001 for both groups). Benomyl (P < 0.05)

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26 L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30

Fig. 1. Trophic structure (proportion in %) of the nematode fauna at the heath and the fellfield at different soil depths. For treatment codesee Table 1.

reduced the proportion of bacterial feeders, whereasfungal feeders increased with carbon (P < 0.05). Ob-ligate plant parasites increased with benomyl aloneand in combination with fertilizer or bactericides (P <

0.05), and omnivores decreased in all treated plots ex-cept for the bactericide treatment (P < 0.001 for C,F, B and all combinations). The occurrence of plantfeeders was unaffected by the manipulations.

The trophic diversity (T) at the heath at 0–6 cmdepth ranged between 1.96 and 2.76 (Table 2). In the0–3 cm horizon,T was high in SP, B and F, interme-diate in K and BCF, and low in all other plots. At3–6 cm depth, values were high in SP, C, B and SPB,intermediate in K and low in the other treatments. Anegative main effect of fertilization occurred (P <

0.01). At the fellfield trophic diversity showed a rangefrom 1.61 to 2.77. Diversity was high in the plotsSPB, SP and K, low in BCF, and intermediate in theothers.

4. Discussion

4.1. Species diversity

Nematode species numbers, richness and diver-sity in the control plots were comparable to those ofgrassland or forest soils in temperate regions (Hánel,1996; Ruess, 1995b; de Goede and Bongers, 1998),and are in line with findings of previous studies atsites nearby (Ruess et al., 1998, 1999a,b). This re-markably high diversity of nematodes in habitats athigh latitudes may be an important factor in climat-ically harsh environments. It has been proposed forother communities that functionally redundant speciesmay represent a form of biological insurance againstspecies loss by natural population cycles or distur-bance (McGrady-Steed et al., 1997; Naeem and Li,1997). Further, a species-rich nematode fauna, repre-senting a variety of ecologically different types, will

L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30 27

be able to more efficiently use the limited resourcesin arctic soil systems. This supports the statement ofSohlenius et al. (1997) that nematodes are a majorcomponent of the soil fauna in tundra systems.

Generally, the applied treatments (except the bacte-ricide) resulted in a decrease in nematode biodiversity.Effects were most severe with fungicide treatments un-der nutrient enriched conditions. At both sites richnesswas the most effective index in distinguishing differ-ences, but all other indices were affected by the ex-perimental manipulations also, indicating that they aresensitive tools reflecting the degree of environmentaldisturbance. However, as the occurrence of a nema-tode species is determined by many factors, most ef-fects may be soil specific. Therefore, such indices mayhave limited use as general indicators of any partic-ular soil type, but can be useful discriminators underdefined soil and climatic conditions (Yeates and Bird,1994).

The applications of fungicide and bactericide werean attempt to manipulate the fungal to bacterial ratioin the soil. However, although a decrease in micro-bial biomassC was found in fungicide treated plotsafter 2 years (Michelsen et al., 1999), there was noresponse in microbial biomassC, bacterial and fun-gal biomass after 4 years (Schmidt et al., 2000). Thelow and inconstant effect on the target organisms, thefungi and bacteria, could be due to a high adsorption orlow persistence of pesticides in the organogenic soils.Similarly, to the microbes, the nematode fauna wasnot affected by bactericide application after 4 years.In contrast, nematode species diversity showed a dis-tinct negative response to the fungicide treatment. Asfungal biomass was unchanged it was not the lack ofnematode food supply but rather the direct toxicity ofbenomyl that led to the extinction of several speciesand subsequently to a decrease in diversity. This issupported by the fact that the decline in species num-bers was most pronounced among bacterial feedersand omnivores, whereas the number of fungal feedingspecies was relatively unaffected.

Generally, the nematode fauna showed a lower bio-diversity but a greater response to the treatments atthe climatically harsh high altitude fellfield. This wasprobably partly caused by the fact that the total amountof substances applied per gram of soil was higher atthe fellfield, due to the mere 2 cm thick humus layer.However, similar findings were observed in the experi-

ments on environmental manipulations simulating cli-mate change at field sites nearby (Ruess et al., 1999a),suggesting that nematode populations in arctic soilsexposed to extreme environmental conditions may bemore sensitive to disturbance. This could be a resultof the lower initial biodiversity, i.e. the smaller pool ofredundant species, that could potentially buffer com-munity function in the perturbed soils. Ecosystem pro-cesses may be affected by this low biodiversity, as theyare expected to be more stable in diverse communities(Naeem and Li, 1997).

4.2. Dominance structure

With the amendments of NPK fertilizer and carbonwe aimed to minimize resource limitations for plantsand decomposers in the soil. As expected, plants werestrongly nutrient limited and their biomass increasedat both sites after fertilization, whereas microbialbiomassC increased after carbon supply at the heath,and with carbon combined with fertilizer at the fell-field (Michelsen et al., 1999; Schmidt et al., 2000).The nematode population density reflected these shiftswith a doubling in plots with fertilization alone at theheath, and in combination with the carbon at bothsites (Schmidt et al., 2000). A positive response of ne-matode populations to NPK fertilization has been re-ported in several studies (e.g. Sohlenius and Boström,1986; Aescht and Foissner, 1992; Dmowska andIlieva, 1995; Wasilewska, 1995; Ruess et al., 1999a).This is usually accompanied by changes in species(i.e. richness, diversity) and dominance structure asobserved in the present experiment. Nutrient amend-ment supported general opportunists among the ne-matode fauna, likeAcrobeloidesandAphelenchoides.However, fertilization did not favour all nematodes,as the dominance ofPrismatolaimusat both sites,and additionally ofEudorylaimus, MonhystrellaandProdesmoraat the fellfield, decreased significantly.This could be due to different life-history strate-gies, e.g. nematodes of the genusEudorylaimusareK-strategists and sensitive to disturbance (Bongers,1990). Others may have been out-competed byopportunistic species using the enriched environmen-tal conditions more successfully. Microcosm studiesby Mikola (1998) showed that the positive responseof microbivorous nematodes to increased resourceavailability can be hindered by competition.

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Although measurements of the fungal biomassdid not reveal any effect of the fungicide on tar-get organisms (Schmidt et al., 2000), benomyl wasa strong toxin to non-target organisms. The pop-ulation density of the nematodes was reduced by20–60% and 60–85% compared to the control atheath and fellfield, respectively (Schmidt et al., 2000).The present study showed a change in dominancestructure in favor ofr-strategists. Again the sameopportunistic genera which increased after nutrientenrichment,Acrobeloidesand Aphelenchoides, werefavored by the experimental perturbations. Theseshifts were accompanied by a distinct reduction inboth maturity indices (MI,

∑MI), indicating severe

disturbance. The plant parasite index (PPI) remainedstable, which corresponds to the findings that theplant biomass was unchanged, too (Michelsen et al.,1999).

4.3. Trophic structure

In contrast to the distinct impact of the manipula-tions on abundance, dominance and species structureof the nematode fauna, the trophic structure was onlymoderately affected. Omnivores generally decreasedin the treated plots, probably due to the fact thatspecies in this trophic group all belonged to the sensi-tive K-strategists. Additionally, at the fellfield fungalfeeders increased in proportion in fertilizer or beno-myl treated plots. As the amount of fungal biomassmeasured by the phospholipid fatty acid 18:2v 6, 9generally did not change (Schmidt et al., 2000), theshift in favor of fungal feeders was not related todetectable changes in the nematode food source. Thedominant fungal feeder at both sites was the tolerantgenusAphelenchoides, which increased strongly inproportion, and thereby compensated for the loss ofsensitive species.

The trophic diversity index (T) was relatively un-affected by the manipulations at the heath (exceptfor a negative effect of fertilization at 3–6 cm depth)and moderately reduced at the fellfield. Changes weremainly caused by increases in the fungal to bacte-rial feeders ratio. The latter is used as an index ofrelative availability of food resources and decompo-sition pathways (Freckman and Ettema, 1993; Neherand Campbell, 1994; McSorley, 1997). However, inour experiments the addition of bactericides or fungi-

cides did not significantly change the fungal to bac-terial biomass ratio of the microorganisms (Schmidtet al., 2000). According to this it was not a switch inthe decomposition pathway but the increase of the tox-itolerant opportunistAphelenchoidesthat caused theobserved changes in trophic diversity. For our pur-pose this index has limited usefulness for discerningtrends, due also to the fact that it does not indicatewhich trophic group is dominant. More detailed dataon nematode community composition, such as the in-dices presented above, are required to accurately as-sess environmental disturbances, which is in line withthe conclusions from other studies (McSorley, 1997;Yeates and Bird, 1994).

Changes in functional (trophic) groups of the ne-matode populations were generally minor, in par-ticular at the low altitude heath. This contrastswith the distinct negative effects on species diver-sity and indicates a considerable redundancy amongthe nematode fauna. The biomass responses of mi-croorganisms and plants (e.g. an increase of plantbiomass after fertilization and of microbial biomassafter fertilizer and/or carbon application; no changesafter fungicide treatment; Michelsen et al., 1999;Schmidt et al., 2000) suggest that not all nematodespecies are crucial for the mineralization processesin the investigated soils. In most of the disturbedsoils tolerant species, i.e.Acrobeloidesor Aphelen-choides, increased in numbers, likely compensat-ing for the loss of others. However, we observeddensity compensation only for bacterial and fungalfeeders, whereas the higher trophic level, the omni-vores, was strongly reduced. As population densitygenerally declined after perturbation with beno-myl, no functional compensation occurred at thatplots. Reduced grazing pressure due to lower nema-tode abundance may in turn have affected microor-ganisms and led to a decreased nutrient turn-overas observed in benomyl treated soils (Michelsenet al., 1999). Thus, the trophic group approach canbe a useful tool in soil food web analyses, butconsidering the great changes observed in com-munity structure, it will be inappropriate in nema-tode ecology studies (Ettema, 1998). However, onlymore field studies linking individual species withinthe functional groups to ecosystem processes willshow if faunal diversity is essential for ecosystemfunction.

L. Ruess et al. / Applied Soil Ecology 17 (2001) 19–30 29

5. Conclusions

Environmental manipulation of soils at two con-trasting subarctic sites by nutrient (NPK) and energy(carbon) enrichment or fungicide application resultedin similar responses in the nematode fauna. Gener-ally, biodiversity and maturity indices declined, mostdistinctly with the fungicide benomyl, which was astrong toxin to nematodes. Fungicide addition underenriched conditions was the strongest perturbation tothe nematode fauna. The negative impact of the manip-ulations was most severe at the fellfield site, which isexposed to harsh climatic conditions, suggesting thatsuch habitats are more sensitive to disturbance. Thismay be an important aspect in the context of climatechange at high latitudes.

In contrast to the distinct changes in species di-versity and dominance structure, the trophic structurewas relatively stable to environmental manipulations.Thus, changes within single trophic groups of thesoil food web were greater than within the differ-ent trophic levels of the nematode community. Thisshows that nematode species within a functionalgroup can have quite different life histories and en-vironmental tolerances. However, taking into accountthe estimates of functional properties at the sites (e.g.microbial biomass or plant growth; Michelsen et al.,1999; Schmidt et al., 2000) our results support theconclusions of Setälä et al. (1998) that decompositionprocesses are more sensitive to changes in entire func-tional groups than to manipulations in single specieswithin a group.

Acknowledgements

We are much indebted to S. Esser (Aachen) andto the staff at Abisko Research Station for help dur-ing various stages of the work. Prof. Dr. P. Schmidt(Aachen) is thanked for institutional help. The fieldwork was funded by the Danish Natural Science Re-search Council, grant number 95-01046.

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