Biol Fertil Soils (1999) 28 : 212–218
Q Springer-Verlag 1999
ORIGINAL PAPER
J. Mikola 7 H. Setälä
Interplay of omnivory, energy channels and C availability in a microbial-based soil food web
Received: 15 December 1997
Abstract To study the effects of omnivory on the structure and function of soil food webs and on the control of trophic-level biomasses in soil, two food webs were established in microcosms. The first one contained fungi, bacteria, a fungivorous nematode (Aphelenchoides saprophilus) and a bacterivorous nematode (Caenorhabditis elegans), and the second one fungi, bacteria, the fungivore and an omnivorous nematode (Mesodiplogaster sp.) feeding on both bacteria and the fungivore. Half of the replicates of each food web received additional glucose. The microcosms were sampled destructively at 5, 9, 13 and 19 weeks to estimate the biomass of microbes and nematodes and the soil NH4c-N concentration. The evolution of CO2 was measured to assess microbial respiration. Microbial respiration was increased and soil NH4c-N concentration decreased by the addition of glucose, whereas neither was affected by the food-web structure. Supplementary energy increased the biomass of fungi and the fungivore, but decreased the biomass of bacteria, the bacterivore and the omnivore. The omnivore achieved greater biomass than the bacterivore and reduced the bacterial biomass less than the bacterivore. The biomass of the fungivore was smaller in the presence of the omnivore than in the presence of the bacterivore at three sampling occasions. Fungal biomass was not affected by food-web structure. The results show that the effects of the omnivore were restricted to its resources, whereas more remote organisms and soil processes were not substantially influenced. The results also indicate that the presence of an omnivore does not necessarily alter the control of populations as compared with a food web containing distinct trophic levels, and that the fungal and bacterial channels may respond differently to changes in energy supply. J. Mikola (Y) 7 H. Setälä Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FIN-40351 Jyväskylä, Finland e-mail:
[email protected], Fax: c358-14-602321
Key words Omnivory 7 Soil food web 7 Energy channel 7 Nematode 7 Microbial production
Introduction Omnivorous species, i.e. those feeding on several trophic levels, were earlier thought to be rare in food webs because omnivory makes model food webs locally unstable (Pimm and Lawton 1978) and because real food webs seemed to have less omnivory than one would expect by chance (Pimm 1980). Recent surveys of food webs have, however, revealed that omnivores are common in various habitats (Sprules and Bowerman 1988; Polis 1991), including soils (Walter 1987; Gunn and Cherrett 1993). Law and Blackford (1992) have also shown that model communities containing omnivores are permanent despite being locally unstable, and that species can coexist in these communities. Consequently, omnivores are currently suggested to have substantial effects on trophic interactions within food webs (Sprules and Bowerman 1988; Diehl 1993; Persson et al. 1996; Polis and Strong 1996). Confirming the existence and importance of omnivory in soil food webs, Hyvönen and Persson (1996) recently showed how a diverse group of collembolans and oribatid mites, which usually are considered to be mainly fungivores, were able to reduce the abundance of bacterivorous nematodes. Because omnivory was earlier thought to be rare, trophic-dynamic models, i.e. food-web models based on the concept of trophic levels, paid little attention to omnivory (Oksanen 1991; see however Menge and Sutherland 1976). Basic trophic-dynamic models, when using trophic interactions of the Lotka-Volterra type, predict that: (1) resource availability and predation, i.e. factors that limit biomass at trophic levels, alternate at adjacent levels, and (2) increasing productivity leads to increased biomass only at levels limited by resources (Oksanen et al. 1981). Due to their feeding behaviour omnivores violate the distinctness of trophic levels,
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however, and models with alternating limiting factors at adjacent trophic levels may become irrelevant in communities where a consumer is able to control the biomass of prey at two or more levels (Polis and Holt 1992; Persson, et al. 1996). For instance, in the case of intraguild predation (Fig. 1a) an omnivorous species feeds on both a resource and on a consumer of that resource (Polis and Holt 1992). An example from soil food webs is a mite feeding on both fungi and a fungivorous nematode (Walter 1987). Hairston and Hairston (1997), however, argue that omnivores do not necessarily eliminate trophic-level dynamics in food webs. Their argument is supported by the clear trophic-level dynamics found in aquatic systems dominated by omnivores (Power 1990). Soil food webs are composed of energy channels that originate from bacteria, fungi and plant roots, and that merge at higher trophic levels (Moore and Hunt 1988; Wardle and Yeates 1993). Trophic interactions within channels may differ from each other, for instance due to different responses of bacteria and fungi to microbivore grazing (Wardle and Yeates 1993; Mikola and Setälä 1998a, b). Moreover, together with omnivory, energy channels lead to novel food-web structures. For instance, when a food web contains bacteria, fungi, a fungivore and an omnivore that is capable of feeding on both bacteria and the fungivore, the bacterial channel includes two trophic levels (bacteria – omnivore) while the fungal channel includes three levels (fungi – fungivore – omnivore; Fig. 1b). Since many predatory nematodes are known to feed on both bacteria and microbivorous nematodes (Small 1987; Yeates 1987), this kind of structure should be a common part of soil food webs. To examine the effects of omnivory in soil food webs, we performed a soil microcosm experiment. We established the food web presented in Fig. 1b, as well as a food web including a bacterivore instead of the omnivore, and increased C availability with the addition of glucose in half of the replicates of each food web. The two aims of the experiment were: (1) to clarify the general influence of omnivory on the structure and functioning of food webs in soil; (2) to study whether the control of populations, both in the absence and presence of the omnivore, could be understood by using a
Fig. 1a, b Scheme of simple soil food webs illustrating possible consequences of omnivorous relationships; a omnivory leads to intraguild predation; b omnivory unites energy channels. Food web presented in b was established in the present experiment
basic trophic-dynamic model developed for aboveground food webs (Oksanen et al. 1981).
Materials and methods Soil microcosms The raw humus used in the experiment was collected from a mature pine (Pinus sylvestris) forest under the F layer, in Jyväskylä, Central Finland, sieved through a 1-cm mesh and oven-dried (70 7C for 48 h). Abscissed birch (Betula pubescens) leaves, collected at the same area, were dried, crushed in to small pieces (ca. 25 mm 2 in area) and mixed with the humus so as to give 3% of the total mass of the leaf-humus mixture. Two grams of dry mixture were then placed into 20-ml glass vials. The vials were closed with cellulose plugs and gamma radiated (28 kGy; Kolmiset Oy, Ilomantsi, Finland) to sterilize the soil. After irradiating the soil the pH in distilled water was 4.1, loss on ignition 67.9% of the dry mass, and concentration of NH4c-N 90mg/g dry soil. To obtain a water content of 60% of fresh mass, 3 ml of water (see below) was added to each vial. The water content varied between 56% and 61% during the experiment. Preliminary experiments revealed that the low pH of gamma-radiated soil prevented bacteria from growing in the leaf-humus mixture. Therefore, 20 mg CaCO3 was added per vial, after dissolution in 2 ml of sterilized water, to increase the pH to 4.5 and enable the successful growth of bacteria. Together with CaCO3, a basal 100 mg of glucose was added to each vial to ensure a rapid increase in the microbial biomass.
Inoculation of organisms and addition of glucose We created two food webs aseptically in a laminar-flow chamber by successively introducing organisms of different trophic levels into the microcosms: (1) bacteria plus fungi plus a bacterial- and a fungal-feeding nematode, and (2) bacteria plus fungi plus an omnivorous and a fungal-feeding nematode. The ten species of bacteria originated from the soil or rhizosphere, and the ten species of fungi, growing commonly in plant litter and soil (Pugh 1974; Kjøller and Struw 1982), from spores filtered from the air. The species are listed and their cultivation on agar plates described by Mikola and Setälä (1998a). The microbes, growing on the surface of agar, were scraped with a sterilized knife into a jar filled with sterilized water. After adding 2 ml water with glucose and CaCO3, 1 ml of microbial suspension was added to each microcosm. The vials were then incubated in darkness at a constant temperature of 19 7C. Nematodes were added 1 week after the microbial inoculum. The bacterial feeder, Caenorhabditis elegans, and the omnivore, Mesodiplogaster sp., were raised on diluted Luria agar plates (half of the normal concentration of agar, one quarter of normal nutrients) with Escherichia coli as a food source. The fungal feeder, Aphelenchoides saprophilus, was raised on malt extract agar with the fungus Cladosporium cladosporioides. Nematodes were extracted from agar in a laminar-flow chamber using a sterilized wet-funnel device (Sohlenius 1979). After extraction the specimens of each species were transferred separately from extraction tubes to three jars containing sterilized water. A volume 0.5 ml of each nematode suspension was then added to the appropriate microcosms, resulting in inocula comprising ca. 110, 65 and 470 individuals of C. elegans, Mesodiplogaster sp. and A. saprophilus, respectively. Since microbial growth in soils is often constrained by C availability (Schnürer et al. 1985; Zak et al. 1994) and since glucose has been shown to be one of the main sugar exudates of plant roots (Curl and Truelove 1986), we decided to increase microbial production in our heterotrophic systems by adding glucose. From week 5 onwards, 25 mg of glucose, diluted in 300 ml of sterilized water, was added weekly to vials intended to have higher micro-
214 bial production. The other vials received 300 ml of sterilized water. Sampling procedure Microcosms were sampled destructively 5, 9, 13 and 19 weeks after inoculation with microbes (eight randomly chosen replicates per treatment per date). At each sampling the soil of a microcosm was carefully mixed; 0.2 g (dry mass, d.m.) was used for microbial analysis and 1.8 g (d.m.) for nematode extraction with the wetfunnel technique (Sohlenius 1979). At the last sampling, 0.5 g soil (d.m.) was used for NH4c analysis, and 1.3 g of soil (d.m.) for nematode extraction. The biomass of bacteria and fungi was estimated by measuring the phospholipid fatty acid (PLFA) concentration in the soil (see method in Frostegård et al. 1991; Frostegård and Bååth 1996). The method is based on the characteristic PLFAs in bacteria and fungi (reviewed by Tunlid and White 1992), which can be measured from a single soil sample and used as estimates for bacterial and fungal biomass. To choose the PLFAs that would reliably represent our special groups of bacteria and fungi, we conducted a preliminary experiment (see details in Mikola and Setälä 1998b). The results indicated that bacterial biomass was best indicated by the PLFAs 16 : 1v7t, cy17 : 0, 18 : 1v7 and cy19 : 0, and fungal biomass by the PLFAs 18 : 2v6 and 18 : 1v9. We also took into consideration the fact that after sterilization soil contains PLFAs bound to dead organic matter and, therefore, measured how quickly these PLFAs decompose in soil. We determined the change in the amount of the selected four bacterial and two fungal PLFAs in active fungal and bacterial communities, respectively, and found that the amount of the PLFAs bound to dead organic matter did not decrease during a 3-week incubation. On the other hand, the rapid changes in the concentrations of PLFAs bound to living organic material indicated that these PLFAs decomposed rapidly. We therefore assumed that the stable PLFAs bound to irradiated organic material did not interfere with observations on the relative differences in living microbial biomass between experimental treatments, as also suggested by Janzen et al. (1994), although they complicate the quantification of absolute differences. As reliable conversion factors which could be used to estimate bacterial and fungal biomass from PLFAs are lacking (Haack et al. 1994, Frostegård and Bååth 1996), the biomass of bacteria and fungi is represented by the PLFA concentration in the soil (nmol/g soil d.m.). The calculations of biomass and respiratory metabolism of the nematodes followed those described by Mikola and Setälä (1998a). To measure the concentration of NH4c-N, the soil was extracted in 2 M KCl for 24 h at 3 7C; the suspension was then filtered and the concentration measured photometrically using a standard method (SFS 3032). The concentration of NO3P-N was not measured due to the negligible amounts normally present in the humus layers (Setälä et al. 1990). Using the method presented by Mikola and Setälä (1998a), the evolution of CO2 was measured at each sampling, 5 or 6 days after sugar addition. Microbial respiration was estimated by subtracting the respiration of the nematodes from the community respiration value.
All statistical analyses were performed using the SPSS statistical package (SPSS 1994). Analysis of variance (ANOVA) was used for microbial respiration, NH4c-N concentration and total nematode biomass, while the biomasses of bacteria, fungi, bacterivore/omnivore and fungivore were analysed with multivariate analysis of variance (MANOVA). The homogeneity of variances was checked with Cochran’s C test, and normality with ShapiroWilks’ test. To fulfil the assumptions of ANOVA, some of the variables needed either a logarithmic (NH 4c-N concentration, the biomass of the bacterivore/omnivore, total nematode biomass) or a square-root (microbial respiration) transformation.
Results The bacterial biomass was similar in both communities at week 5, but was subsequently lower in the presence of the bacterivore than in the presence of the omnivore (Fig. 2a, Table 1). Glucose addition decreased the bacterial biomass (Fig. 2a, Table 1). The fungal biomass was not significantly affected by the food-web structure, but was increased by the addition of glucose (Fig. 2b, Table 1). The biomass of the omnivore was greater than that of the bacterivore throughout the experiment (Fig. 3a, Table 1). The supplementary energy source decreased the biomass of both the bacterivore and the omnivore (Fig. 3a, Table 1). By week 5 the omnivore had reduced the biomass of the fungivore as compared with its biomass in the presence of the bacterivore (Fig. 3b, Table 1). Later on the fungivore biomass was significantly increased by the additional energy source, but was no longer straight-forwardly affected by the foodweb structure (Fig. 3b, Table 1). The significant interaction between food-web structure and time (Table 1) indicated that the structure did affect fungivore biomass, but differently at different samplings. We therefore analysed the data from each sampling separately and found that at weeks 9 and 19 the biomass of the fungivore was significantly lower in the presence of the omnivore than in the presence of the bacterivore (two-way ANOVA; Fp7.79, Pp0.009 and Fp8.32, Pp0.007, re-
Experimental design and statistical analyses The experiment was divided into two parts: before and after the beginning of the addition of glucose at week 5. The first part of the experiment, before the first glucose addition, provided background data for the latter part of the experiment, and its experimental design simply consisted of the factor food web structure with two factor levels: bacterivore and omnivore. The design of the latter part of the experiment consisted of three factors: food web structure, energy addition, and time. Energy addition had two factor levels: control and sugar addition, and time had three levels: 9, 13 and 19 weeks from the establishment of the experiment.
Fig. 2a, b Concentration of phospholipid fatty acids (PLFA) of microbial origin in soil (meanB1 SE) representing the biomass of microbes; a bacterial PLFAs, and b fungal PLFAs in the presence of the bacterivore (B) and the omnivore (O), with an additional energy source present (E) or absent (C). d.m. Dry matter
215 Table 1 Multivariate (Wilks’ lambda) and univariate F statistics of multivariate ANOVA of microbial and nematode biomass in the two food webs at week 5 and between weeks 9 and 19. FWS Food-web structure, EA energy (glucose) addition Week 5
Wilks’ lambda a
Source of variation
df
Food web structure
(4,11)
Weeks 9–19
F
Bacteria
P
5.93
df 0.009
b
(1,14)
F
P
~0.01
0.952
Wilks’ lambda
Fungi F 1.04
Bacteria
Source of variation
df a
F
P
df b
FWS EA Time FWS!EA FWS!time EA!time FWS!EA!time
(4,77) (4,77) (8,154) (4,77) (8,154) (8,154) (8,154)
16.70 90.13 15.48 0.95 5.02 4.24 1.58
~0.001 ~0.001 ~0.001 0.439 ~0.001 ~0.001 0.135
(1,80) (1,80) (2,80) (1,80) (2,80) (2,80) (2,80)
F 4.04 7.74 1.85 0.83 0.76 1.77 0.10
a
P
Bacterivore/omnivore F
0.324 Fungi
P
F 0.001 c
16.51
Fungivore P
13.80
Bacterivore/omnivore
0.002
Fungivore
P
F
P
F
P
F
P
0.048 0.007 0.163 0.364 0.470 0.177 0.902
0.97 92.62 1.24 2.00 2.03 8.08 1.08
0.327 ~0.001 0.295 0.161 0.138 0.001 0.344
54.03 143.94 28.88 0.29 8.50 0.83 2.74
~0.001 c ~0.001 ~0.001 0.590 d ~0.001 d 0.438 0.070 d
1.84 7.34 35.39 0.10 13.33 0.08 0.76
0.179 0.008 ~0.001 0.757 ~0.001 0.921 0.470
df (Treatment, error) for multivariate analysis df (Treatment, error) for univariate analyses c Tests whether the biomasses of omnivore and bacterivore differ
d Tests whether the treatment effect differs between the bacterivore and omnivore
Fig. 3a, b Biomass of nematodes (meanB1 SE); a biomass of the bacterivore (B) and the omnivore (O), with an additional energy source present (E) or absent (C); b biomass of the fungivore in the presence of the bacterivore (B) and the omnivore (O), with an additional energy source present (E) or absent (C)
Fig. 4 Microbial respiration (meanB1 SE) in the presence of the bacterivore (B) and the omnivore (O), with an additional energy source present (E) or absent (C)
spectively), whereas at week 13 it was significantly higher (two-way ANOVA; Fp13.04, Pp0.001). At the last sampling the total biomass of nematodes was not affected by food-web structure or glucose addition (two-way ANOVA; Fp1.52, Pp0.229 and Fp0.77, Pp0.387, respectively). The microbial respiration rate was lower at week 5 in the presence of the omnivore than in the presence of the bacterivore (one-way ANOVA; Fp5.51, Pp0.034; see Fig. 4). Subsequently, the microbial respiration rate was no longer affected by the food-web structure (three-way ANOVA; Fp1.24, Pp0.268), but was clearly increased by the addition of glucose (three-way ANOVA; Fp3982.17, P~0.001; see Fig. 4). During the experiment the soil NH4c-N concentration decreased from 90 mg/g dry soil to ca. 0.5 mg/g dry soil in the food webs provided with glucose, whereas it increased to ca.
115 mg/g dry soil in the food webs without the addition of glucose (Fig. 5). The food-web structure did not affect the NH4c-N concentration at the end of the experiment (two-way ANOVA; Fp1.11, Pp0.300).
b
Discussion As expected, the supplementary source of energy increased the rate of microbial respiration, indicating that microbial production generally increased. Unexpectedly, however, the biomass of bacteria and the bacterivore decreased, and only the biomass of fungi and the fungivore increased, which suggests that only fungal production was stimulated by the additional source of energy. Contrary to the present results, we previously found that adding glucose to soil increases the produc-
216
Fig. 5 Soil NH4c-N concentration (meanB1 SE) at the end of the experiment, in the presence of the bacterivore (B) and the omnivore (O), with an additional energy source present (E) or absent (C)
tion of both bacteria and fungi (Mikola and Setälä 1998b). However, in the present experiment the quantity of glucose was 5 times that used in the latter experiment; this possibly led to such small nutrient concentrations in the soil, as microbes immobilised nutrients to be able to utilise the added source of energy, that only fungi, probably through their hyphae, were able to use the scanty nutrients remaining. Bååth et al. (1978) similarly found that although the fungal biomass was increased in soil by glucose addition, both glucose and N were required to increase the bacterial biomass. Influence of the omnivore on food-web structure and function Although the omnivore produced a greater biomass than the bacterivore, the bacterial biomass was reduced to a larger extent by the bacterivore. Logical explanations for this are that the omnivore attained a greater biomass because it could exploit both energy channels, and that it consumed fewer bacteria because it obtained a substantial part of its energy from the fungal channel. It is possible, however, that differences in the biomasses of the nematodes and bacteria also originated from other differences between the two nematode species than simply omnivory vs. bacterivory. Therefore, we can only propose that the omnivorous feeding habit, when compared with true bacterivory, leads to a greater population density of the grazer and reduced grazing pressure on bacteria. Because the omnivore was able to exploit both energy channels, it should have been less harmed by the decreased bacterial production than the bacterivore. However, both species were practically extinct at the last sampling in the food webs provided with energy. This implies that Mesodiplogaster was unable to compensate for the deficiency of bacteria by feeding exclusively on nematodes, i.e. that bacteria were a necessary resource for it (note that a part of the PLFAs is bound to dead organic matter, which means
that the actual decrease in the living bacterial biomass is much greater than the decrease in the PLFA concentration). Species of Mesodiplogaster have been shown to feed on protozoa and other species of nematodes, in addition to feeding on bacteria (Sohlenius 1968; Elliott et al. 1980). Consistent with the omnivorous nature of Mesodiplogaster, the biomass of the fungivore was significantly smaller in the presence of Mesodiplogaster than in the presence of the bacterivore at three samplings of the present experiment. At one sampling, however, a reverse pattern of fungivore biomass occurred, which implies that, besides affecting the biomass of the fungivore, the omnivore also changed the dynamics of the fungivore population. Fungal biomass was clearly affected by glucose addition but not by changes in the fungivore biomass, which confirms the earlier findings according to which fungal biomass is mainly controlled by the availability of resources (Wardle and Yeates 1993; Mikola and Setälä 1998a, b). Microbial respiration was generally not affected by food-web structure, supporting earlier findings that microbial respiration is not sensitive to modest changes in the biomass of microbial grazers in food webs composed of microbes and nematodes (Mikola and Setälä 1998a, b). Earlier findings that the NH4c-N concentration in soil is determined by the total microbivore biomass (Bouwman et al. 1994; Mikola and Setälä 1998a) were also supported by the fact that neither the total biomass of nematodes nor the NH4c-N concentration was affected by food-web structure at the last sampling of the experiment. To conclude the effects of omnivory on the structure and function of the studied food web, it seems that the effects of the omnivore were mostly restricted to its resources, i.e. to the biomass of bacteria and the fungivore. More remote organisms, i.e. fungi, and soil processes were not substantially influenced. Since omnivory in our experiment did not induce intraguild predation, and since our results were obtained in a smallscale microcosm experiment, comparisons with earlier studies dealing with omnivory (e.g. Polis and McCormick 1987; Spiller and Schoener 1994; Diehl 1995) are not straightforward. Nevertheless, one aspect of our results may be of relevance to intraguild predation, namely that the omnivore was more dependent on the lower-level resource (bacteria) than on the intermediate consumer (fungivore). Omnivory and control of trophic-level biomasses The predictions provided by formal trophic-dynamic models, such as that of Oksanen et al. (1981), can be rigorously tested only when food webs attain a stable state. Because the supplementary energy source did not increase the biomass of both bacteria and fungi in our experiment, the biomass of fungi and the fungivore increased and the biomass of bacteria and the bacterial
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feeding nematodes decreased till the end of the experiment. Thus, biomasses of all organisms displayed transient dynamics. When interpreting these results to provide evidence for or against the Oksanen et al. (1981) model one must therefore be cautious. According to the Oksanen et al. (1981) model, the number of trophic levels in a food chain is an important determinant of its response to changes in productivity. In a two-level system, the biomass at the first trophic level should be limited by predation and the biomass at the second level by resources. Therefore, only the second-level biomass should respond when productivity changes (Oksanen et al. 1981). Our results did not support this prediction, for in the food web without the omnivore the biomass of fungi and the fungivore increased and the biomass of bacteria and the bacterivore decreased when glucose was added. The biomasses of both the microbes and the microbivores were thus limited by resources, which means that resource availability and predation, as limiting factors, did not alternate at adjacent trophic levels. The differences in the fungivore biomass between the two food webs were not reflected in the fungal biomass, which supports earlier findings that trophic cascades of biomass limitation (sensu Oksanen et al. 1981; Carpenter et al. 1985) are rare in microbial-based soil food webs (Mikola and Setälä 1998a). As a result, although omnivores could generally alter biomass control at upper trophic levels of microbial-based food webs, microbes at the lowest level would not probably respond to these changes. The Oksanen et al. (1981) model predicts that the biomass of fungi and the fungivore should respond differently to the changes in productivity in the two food webs since the omnivore forms a third trophic level in the fungal channel. However, as was expected on the basis of the dynamic influence of the omnivore on the fungivore biomass and the absence of the trophic cascade of biomass limitation, the omnivore had no influence on the response of the fungal channel to increased productivity. Consequently, the food webs did not respond to the changes in microbial production as predicted by the Oksanen et al. (1981) model. However, this was attributed to another characteristic of the soil food web rather than omnivory, i.e. to the inability of microbivores to effectively control their resources. Although the present experiment cannot provide unequivocal evidence that the Oksanen et al. (1981) model does not apply to microbial-based soil food webs due to transient biomass dynamics, the results support earlier findings that all trophic levels within these soil food webs respond to changes in bottom-level production parallel to each other (Mikola and Setälä 1998b). In the light of trophic-level dynamics the results imply that; (1) the presence of an omnivore in a food web does not necessarily alter the controlling factors of populations when compared with a food web containing distinct trophic levels (in the present experiment the biomass of fungi, bacteria and the fungivore were
clearly limited by the availability of resources regardless of the presence of the omnivore), (2) the fungal and bacterial channels may respond differently to changes in the energy supply, and (3) within a channel all levels tend to respond to changes in bottom-level production parallel to each other. Acknowledgements We thank the following for providing the organisms used in the experiment: S. Elo for bacteria, M. Käpylä for fungi, B. Sohlenius for the omnivore, W. Traunspurger for the bacterivore, and R. de Goede for the fungivore. A. Mecklin carried out the PLFA analyses, and M. Karppanen and T. Räisänen helped with samplings and nematode counting. The study was financially supported by the Jenny and Antti Wihuri Foundation, the Finnish Cultural Foundation, and the Academy of Finland.
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