Abstract
A major question in soil ecology is whether soil food webs are regulated by resources or by predators, i.e. bottom–up (donor) or top–down controlled. We tested the hypothesis that meso- and macrofaunal soil predators can regulate fungivore populations and, thereby cause a top–down cascade effect on fungal biomass and decomposition/mineralisation processes in boreal forest soils. The study was performed as a microcosm experiment with two contrasting soils (humus layers), one poor and one rich in N, and with different combinations of fungivore and predator soil fauna added to “defaunated” soil. In comparison with control microcosms lacking mesofauna (but with nematodes and protozoans), the presence of a diverse Collembola and Oribatida fungivore community significantly reduced the FDA-active fungal biomass or tended to reduce the ergosterol fraction of the fungal biomass in the N-poor humus, but no clear effect could be detected in the N-rich humus. Fungivores as well as fungivores plus predators (a predator community consisting of gamasids, spiders and beetles or a subset thereof) reduced C mineralisation and increased net N mineralisation in both soils. The presence of predators (particularly gamasid mites) reduced collembolan numbers and alleviated the negative effect of fungivores on fungal biomass in the N-poor soil. In the N-rich soil, the presence of predators increased fungal biomass (ergosterol) in relation to the “defaunated” soil. Therefore, a top–down trophic cascade could be detected in the N-poor humus but not in the N-rich humus. Our results suggest that the degree of top–down control in soil fauna communities depends on resource quality and soil fertility.
Similar content being viewed by others
References
Bååth E, Nilsson LO, Göransson H, Wallander H (2004) Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil? Soil Biol Biochem 36:2105–2109
Balogh J (1972) The oribatid genera of the world. Akadémiai kiadó, Budapest
Bengtsson J, Zheng DW, Ågren GI, Persson T (1995). Food webs in soil: an interface between population and ecosystem ecology. In: Jones CG, Lawton JH (eds) Linking species and ecosystems. Chapman and Hall, London, pp 159–165
Bengtsson J, Lundkvist H, Saetre P, Sohlenius B, Solbreck B (1998) Effects of organic matter removal on the soil food web: forestry practices meet ecological theory. Appl Soil Ecol 9:137–143
Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setälä H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–618
Clarholm M (1985) Possible roles of roots, bacteria, protozoa and fungi in supplying nitrogen to plants. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soils. Blackwell Scientific, Oxford, pp 355–366
Faber JH, Verhoef HA (1991) Functional differences between closely related soil arthropods with respect to decomposition processes in the presence or absence of pine roots. Soil Biol Biochem 23:15–24
Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–409
Fjellberg A (1980) Identification keys to Norwegian collembola. The Norwegian Entomological Society, Ås
Fjellberg A (1998) The collembola of Fennoscandia and Denmark. I: Poduromorpha and onychiuridae. Fauna ent Scand 35:184
Frankland JC (1998) Fungal succession—unravelling the unpredictable. Mycol Res 102:1–15
Gilyarov MS, Krivolutsky DA (1975) A key to soil-inhabiting mites. Sarcoptiformes. Izdatel´stvo Nauka, Moscow (In Russian)
Hanlon RDG (1981) Influence of grazing by collembola on the activity of senescent fungal colonies grown on media of different nutrient concentration. Oikos 36:362–367
Hedlund K, Sjögren Öhrn M (2000) Tritrophic interactions in a soil community enhance decomposition rates. Oikos 88:585–591
Hyvönen R, Persson T (1996) Effects of fungivorous and predatory arthropods on nematodes and tardigrades in microcosms with coniferous forest soil. Biol Fertil Soils 21:121–127
Kandeler E, Kampichler C, Joergensen RG, Mölter K (1999) Effects of mesofauna in a spruce forest on soil microbial communities and N cycling in field mesocosms. Soil Biol Biochem 31:1783–1792
Kareiva P (1989) Renewing the dialogue between theory and experiments in population ecology. In: Roughgarden J, May RM, Levin SA (eds) Perspectives in ecological theory. Princeton University Press, Princeton, New Jersey
Kårén O, Nylund JE (1996) Effects of N-free fertilization on ectomycorrhiza community structure in Norway spruce stands in southern Sweden. Plant Soil 181:295–305
Karg W (1993) Acari (Acarina), Milben Parasitiformes (Anactinochaeta), Cohors Gamasina Leach, Raubmilben. Die Tierwelt Deutschlands 59
Karg W (1994) Raubmilben, nützliche Regulatoren im Naturhaushalt. Neue Brehm Bücherei 624:206
Klamer M, Hedlund K (2004) Fungal diversity in set-aside agricultural soil investigated using terminal-restriction fragment length polymorphism. Soil Biol Biochem 36:983–988
Koehler HH (1999) Predatory mites (Gamasina, Mesostigmata). Agric Ecosyst Environ 74:395–410
Laakso J, Setälä H (1999) Population- and ecosystem-level effects of predation on microbial-feeding nematodes. Oecologia 120:279–286
Leps J, Brown VK, Diaz Len TA, Gormsen D, Hedlund K, Kailová J, Korthals GW, Mortimer SR, Rodriguez-Burrueco C, Roy J, Santa Regina I, Van Dijk C, Van der Putten WH (2001) Separating the chance effect from other diversity effects in the functioning of plant communities. Oikos 92:123–134
Liiri M, Setälä H, Haimi J, Pennanen T, Fritze H (2002). Soil processes are not influenced by the functional complexity of soil decomposer food webs under disturbance. Soil Biol Biochem 34:1009–1020
Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of micro- and mesobiota in below-ground detrital food webs. Ann Rev Entom 33:419–439
Nylund J-E, Wallander H (1992) Ergosterol analysis as a means of quantifying mycorrhizal biomass. In: Norris JR, Read DJ, Varma AK (eds) Methods Microbiol 24:77–88
Osenberg CW, Mittelbach GG (1996) The relative importance of resource limitation and predator limitation in food web chains. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman & Hall, New York, pp 134–148
Persson T (1989) Role of soil animals in C and N mineralization. Plant Soil 115:241–245
Persson T, Wirén A (1993) Effects of experimental acidification on C and N mineralization in forest soils. Agric Ecosyst Environ 47:159–174
Persson T, Bååth E, Clarholm M, Lundkvist H, Söderström, BE, Sohlenius B (1980) Trophic structure, biomass dynamics and carbon metabolism of soil organisms in a Scots pine forest. Ecol Bull (Stockholm) 32:419–459
Persson T, Lundkvist H, Wirén A, Hyvönen R, Wessén B (1989) Effects of acidification and liming on carbon and nitrogen mineralization and soil organisms in mor humus. Water Air Soil Pollut 45:77–96
Persson L, Bengtsson J, Menge B, Power M (1995) Productivity and consumer regulation—concepts, patterns and mechanisms. In: Polis G, Winemiller K (eds) Food webs: patterns and processes. Chapman & Hall, London, pp 396–434
Persson T, Rudebeck A, Jussy JH, Colin-Belgrand M, Priemé A, Dambrine E, Karlsson PS, Sjöberg RM (2000) Soil nitrogen turnover—mineralisation, nitrification and denitrification in European forest soils. In: Schulze E-D (ed) Carbon and nitrogen cycling in European forest ecosystems. Ecol Stud 142:297–331
Petersen JE, Hastings A (2001) Dimensional approaches to scaling experimental ecosystems: designing mousetraps to catch elephants. Am Nat 157:324–333
Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846
Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J (2000) When is a trophic cascade a trophic cascade? TREE 15:473–475
Rudebeck A, Persson T (1998) Nitrification in organic and mineral soil layers in coniferous forests in response to acidity. Environ Pollut 102:377–383
Santos PF, Phillips J, Whitford WG (1981) The role of mites and nematodes in early stages of buried litter decomposition in a desert. Ecology 62:664–669
Scheu S (2002) The soil food web: structure and perspectives. Eur J Soil Biol 38:11–20
Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153
Seastedt TR (1984) The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46
Setälä H (1995) Growth of birch and pine seedlings in relation to grazing by soil fauna on ectomycorrhizal fungi. Ecology 76:1844–1851
Setälä H, Huhta V (1992) Soil fauna increase Betula pendula growth: laboratory experiments with coniferous forest floor. Ecology 72:665–671
Setälä H, Tyynismaa M, Martikainen E, Huhta V (1991) Mineralisation of C, N and P in relation to decomposer community structure in coniferous forest soils. Pedobiologia 35:285–296
Siepel H, de Ruiter-Dijkman EM (1993) Feeding guilds of oribatid mites based on their carbohydrase activities. Soil Biol Biochem 25:1491–1497
Smith VC, Bradford MA (2003) Litter quality impacts on grassland litter decomposition are differently dependent on soil fauna across time. Appl Soil Ecol 24:197–203
Söderström BE (1977) Vital staining of fungi in pure culture and in soil with fluorescein diacetate. Soil Biol Biochem 9:59–63
Söderström B, Erland S (1986) Isolation of fluorescein diacetate stained hyphae from soil by micromanipulation. Trans Br Mycol Soc 86:465–468
Sohlenius B (1990) Influence of cropping system and nitrogen input on soil fauna and microorganisms in a Swedish arable soil. Biol Fertil Soils 9:168–173
Strong DS (1992) Are trophic cascades all wet? Differentiation and donor control in speciose ecosystems. Ecology 73:747–754
Sulkava P, Huhta V, Laakso J (1996) Impact of soil faunal structure on decomposition and N-mineralisation in relation to temperature and moisture in forest soil. Pedobiologia 40:505–513
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Studies in ecology, vol 5. Blackwell, Oxford, pp 372
Valiela I, Rutecki D, Fox S (2004) Salt marshes: biological controls of food webs in a diminishing environment. J Exp Mar Biol Ecol 300:131–159
Van der Drift J, Jansen E (1977) Grazing of springtails on hyphal mats and its influence on fungal growth and respiration. Ecol Bull (Stockholm) 25:203–209
Van de Koppel J, Bardgett RD, Bengtsson J, Rodriguez-Barrueco C, Rietkerk M, Wassen M, Wolters V (2005) The effects of spatial scale on trophic interactions. Ecosystems 8:801–809
Villenave C, Ekschmitt K, Nazaret S, Bongers T (2004) Interactions between nematodes and microbial communities in a tropical soil following manipulation of soil food web. Soil Biol Biochem 36:2033–2043
Willmann C (1931) Moosmilben oder Oribatiden (Oribatei). Die Tierwelt Deutschlands 22:70–196
Wyman RL (1998) Experimental assessment of salamanders as predators of detrital food webs: effects on invertebrates, decomposition and carbon cycle. Biodivers Conserv 7:641–650
Zheng DW, Bengtsson J, Ågren GI (1997) Soil food webs and ecosystem processes: decomposition in donor-control and Lotka–Volterra systems. Am Nat 149:125–148
Zheng DW, Ågren GI, Bengtsson J (1999) How do soil organisms affect total organic nitrogen storage in soils and substrate nitrogen to carbon ratio? A theoretical analysis. Oikos 86:430–442
Acknowledgements
Grants for the study were received from the Swedish Council for Forestry and Agricultural Research, SJFR (TP), Swedish Natural Science Research Council, NFR (JB) and the Erasmus program (LL).
Author information
Authors and Affiliations
Corresponding author
Appendices
Appendix 1
Mean number (no. g−1 dry weight) of “fungivores” (collembolans and oribatids) in control soil (0) obtained after 50 and 100 days in the following five treatments: F=fungivores, P=fungivores + predators, G=fungivores + gamasid mites, S=fungivores + spiders, B=fungivores + beetles. *The estimates of F on day 50 were based on much smaller samples than the other treatments (4 g vs 20 g) resulting in uneven species composition. Values for 50 days for Collembola have been corrected for differences in extraction efficiency, and are not the same as in Fig. 1.
Appendix 2
Mean number (no. g−1 dry weight) of “fungivores” (collembolans and oribatids) in fertilised soil (N) obtained after 50 and 100 days. See “Appendix 1” for details.
Rights and permissions
About this article
Cite this article
Lenoir, L., Persson, T., Bengtsson, J. et al. Bottom–up or top–down control in forest soil microcosms? Effects of soil fauna on fungal biomass and C/N mineralisation. Biol Fertil Soils 43, 281–294 (2007). https://doi.org/10.1007/s00374-006-0103-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-006-0103-8