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Trophic guilds of generalist feeders in soil animal communities as indicated by stable isotope analysis (15N/14N)

Published online by Cambridge University Press:  29 January 2010

K. Oelbermann
Affiliation:
Darmstadt University of Technology, Institute of Zoology, Schnittspahnstr. 3, 64287Darmstadt, Germany
S. Scheu*
Affiliation:
Georg-August-University Göttingen, J.F. Blumenbach Institute of Zoology and Anthropology, Berliner Str. 28, 37073Göttingen, Germany
*
*Author for correspondence Fax: 0049-551-395448 E-mail: sscheu@gwdg.de

Abstract

We investigated if the commonly used aggregation of organisms into trophic guilds, such as detritivores and predators, in fact represent distinct trophic levels. Soil arthropods of a forest-meadow transect were ascribed a priori to trophic guilds (herbivores, detritivores, predators and necrovores), which are often used as an equivalent to trophic levels. We analysed natural variations in 15N/14N ratios of the animals in order to investigate the trophic similarity of organisms within (a priori defined) trophic guilds. Using trophic guilds as an equivalent to trophic level, the assumed stepwise enrichment of 15N by 3.4‰ per trophic level did not apply to detritivores; they were only enriched in 15N by on average 1.5‰ compared to litter materials. Predators on average were enriched in 15N by 3.5‰ compared to detritivores. Within detritvores and predators δ15N signatures varied markedly, indicating that these trophic guilds are dominated by generalist feeders which form a gradient of organisms feeding on different resources. The results indicate that commonly used trophic guilds, in particular detritivores and predators, do not represent trophic levels but consist of subguilds, i.e. subsets of organisms differing in resource utilization. In particular, in soil and litter food webs where trophic level omnivory is common, the use of distinct trophic levels may be inappropriate. Guilds of species delineated by natural variations of stable isotope ratios are assumed to more adequately represent the structure of litter and soil food webs allowing a more detailed understanding of their functioning.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2010

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References

Albers, D., Schaefer, M. & Scheu, S. (2006) Incorporation of plant carbon into the soil animal food web of an arable system. Ecology 87, 235245.Google Scholar
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. Applied Soil Ecology 9, 137143.CrossRefGoogle Scholar
Blower, J.G. (1985) Millipedes. Synopses of the British Fauna (New Series) 35. London, Brill Backhuys.Google Scholar
Briones, M.J.I., Ineson, P. & Sleep, D. (1999) Use of δ13C to determine food selection in collembolan species. Soil Biology and Biochemistry 31, 937940.Google Scholar
Chahartaghi, M., Langel, R., Scheu, S. & Ruess, L. (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biology and Biochemistry 37, 17181725.CrossRefGoogle Scholar
Chen, B., Snider, R.J. & Snider, R.M. (1996) Food consumption by Collembola from northern Michigan deciduous forest. Pedobiologia 40, 149161.CrossRefGoogle Scholar
Chinery, M. (1993) Parey's Buch der Insekten. Hamburg and Berlin, Germany, Verlag Paul Parey.Google Scholar
Coleman, D.C. & Crossley, D.A. (1996) Fundamentals of Soil Ecology. San Diego, California, USA, Academic Press.Google Scholar
De Ruiter, P.C., Neutel, A.M. & Moore, J.C. (1996) Energetics and stability in below-ground food webs. pp. 201210in Polis, G.A. & Winemiller, K.O. (Eds) Food Webs. Integration of Patterns and Dynamics. New York, USA, Chapman and Hall.Google Scholar
Dücker, A., Schmüser, H., Heubel, K., Borcherding, R., Heubel, V., Müller-Reich, C., Pahnke, K., Gienapp, P., Nötzold, R. & Nötzold, V. (1997) Laufkäfer. Hamburg, Germany, Deutscher Jugendbund für Naturbeobachtung.Google Scholar
Dunger, W. (1983) Tiere im Boden. 3. Auflage. Neue Brehm-Bücherei. A. Wittenberg Lutherstadt, Germany, Ziemsen-Verlag.Google Scholar
Eisenbeis, G. & Wichard, W. (1985) Atlas zur Biologie der Bodenarthropoden. Stuttgart, Germany, Gustav Fischer Verlag.Google Scholar
Ernsting, G. (1977) Aspects of predation and the coexistence of collembolan prey species. Ecological Bulletins (Stockholm) 25, 478480.Google Scholar
Ernsting, G., Isaaks, J.A. & Berg, M.P. (1992) Life cycle and food availability indices in Notiophilus biguttatus (Coleoptera, Carabidae). Ecological Entomology 17, 3342.CrossRefGoogle Scholar
Fisler, J.S., Drenick, E.J., Blumfeld, D.E. & Swendseid, M.E. (1982) Nitrogen economy during very low calorie and very low protein diets. American Journal of Clinical Nutrition 35, 471486.Google Scholar
Fjellberg, A. (1980) Identification keys to the Norwegian Collembola. Ås, Norway, Norsk Entomologisk Forening.Google Scholar
Freude, H., Harde, K.W. & Lohse, G.A. (1976) Die Käfer Mitteleuropas, Band 2 Adephaga 1. Krefeld, Germany, Goecke & Evers.Google Scholar
Gannes, L.Z., O'Brien, D.M. & Martinez del Rio, C. (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 12711276.CrossRefGoogle Scholar
Hairston, N.G. & Hairston, N.G. (1993) Cause-effect relationships in energy flow trophic structure, and interspecific interactions. The American Naturalist 142, 379411.Google Scholar
Halaj, J. & Wise, D.H. (2002) Impact of detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83, 31413151.CrossRefGoogle Scholar
Handley, L.L. & Scrimgeour, C.M. (1997) Terrestrial plant ecology and 15-N natural abundance: the present limits to interpredation for uncultivated systems with original data from a Scottish old field. Advances in Ecological Research 27, 139212.Google Scholar
Harde, K.W. & Severa, F. (1998) Der Kosmos-Käferführer. Stuttgart, Germany, Franckh'sche Verlagsbuchhandlung.Google Scholar
Heimer, S. & Nentwig, W. (1991) Spinnen Mitteleuropas. Berlin, Germany, Paul Parey.Google Scholar
Honomichl, K. (1998) Jacobs/Renner-Biologie und Ökologie der Insekten. 3.Auflage. Stuttgart, Germany, Gustav Fischer.Google Scholar
Hopkin, S.P. & Read, H.J. (1992) The Biology of Millipedes. New York, USA, Oxford University Press.Google Scholar
Hövemeyer, K. (1999) Abundance patterns in terrestrial dipteran communities. Pedobiologia 43, 2843.CrossRefGoogle Scholar
Hunt, H.W., Coleman, D.C., Ingham, E.R., Inham, R.E., Elliott, E.T., Moore, J.C., Rose, S.L., Reid, C.P.P. & Morley, C.R. (1987) The detrital food web in a shortgrass prairie. Biology and Fertility of Soils 3, 5768.Google Scholar
Jones, D. (1990) Der Kosmos-Spinnenführer. Mitteleuropäische Spinnen und Weberknechte. Stuttgart, Germany, Kosmos-Franckh'sche Verlagsbuchhandlung.Google Scholar
Locket, G.H. & Millidge, A.F. (1951) British Spiders, Vol. I, II. London, UK, Ray Society.Google Scholar
McNabb, D.M., Halaj, J. & Wise, D.H. (2001) Inferring trophic positions of generalist predators and their linkage to the detrital food web in agroecosystems: a stable isotope analysis. Pedobiologia 45, 289297.Google Scholar
Minagawa, M. & Wada, E. (1984) Stepwise enrichment of 15N along food chains: Further evidence and the relation between Delta 15N and animal age. Geochimica et Cosmochimica Acta 48, 11351140.CrossRefGoogle Scholar
Moore, J.C. & De Ruiter, P.C. (1991) Temporal and spatial heterogeneity of trophic interactions within below-ground food webs. Agriculture Ecosystems and Environment 34, 371397.Google Scholar
Nadelhoffer, K.J. & Fry, B. (1988) Controls of nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Science Society of America Journal 52, 16331640.CrossRefGoogle Scholar
Neilson, R., Hamilton, D., Wishart, J., Marriotti, C.A., Boag, L., Handley, L.L., Scrimgeour, C.M., McNicol, J.W. & Robinson, D. (1998) Stable isotope natural abundances of soil, plants and soil invertebrates in an upland pasture. Soil Biology and Biochemistry 30, 17731782.Google Scholar
Nyffeler, M., Sterlling, W.L. & Dean, D.A. (1994) How spiders make a living. Environmental Entomology 23, 13571367.CrossRefGoogle Scholar
Oelbermann, K., Langel, R. & Scheu, S. (2008) Utilization of prey from the decomposer system by predators of grassland. Oecologia 155, 605617.CrossRefGoogle ScholarPubMed
Ostrom, P.H., Colunga-Garcia, M. & Gage, S.H. (1997) Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109, 108113.Google Scholar
Peterson, B.J. & Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293320.Google Scholar
Pearson, S.F., Levey, D.J., Greenberg, C.H. & Martinez del Rio, C. (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135, 516523.CrossRefGoogle Scholar
Polis, G.A. (1991) Complex trophic interactions in deserts: an empirical critique of food-web theory. The American Naturalist 138, 123155.Google Scholar
Polis, G.A. & Strong, D.R. (1996) Food web complexity and community dynamics. The American Naturalist 147, 813846.Google Scholar
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Reviews of Ecology and Systematics 20, 297330.Google Scholar
Pollierer, M., Langel, R., Scheu, S. & Maraun, M. (2009) Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). Soil Biology and Biochemistry 41, 12211226.CrossRefGoogle Scholar
Ponsard, S. & Arditi, R. (2000) What can stable isotopes (delta 15N and delta 13C) tell about the food web of soil macro-invertebrates? Ecology 81, 852864.Google Scholar
Post, D.M. (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83, 703718.Google Scholar
Reineking, A., Langel, R. & Schikowski, J. (1993) 15N, 13C-on-line-measurements with an elemental analyser (Carlo Erba, NA 1500), a modified trapping box and a gas isotope mass spectrometer (Finnigan, MAT 251). Isotopenpraxis Environmental Health Studies 29, 169174.CrossRefGoogle Scholar
Roberts, M.J. (1995) Collins Field Guide. Spiders of Britain and Northern Europe. London, UK, HarperCollins Publishers.Google Scholar
Rusek, J. (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodiversity and Conservation 7, 12071219.CrossRefGoogle Scholar
Sauer, F. (1996) Wanzen und Zikaden. Karlsfeld, Germany, Fauna-Verlag.Google Scholar
Sauer, F. (1998) Fliegen und Mücken. Karlsfeld, Germany, Fauna-Verlag.Google Scholar
Schaefer, M. (1990) The soil fauna of a beech forest on limestone: trophic structure and energy budget. Oecologia 82, 128136.Google Scholar
Schaefer, M. (1991) The animal community: diversity and resources. pp. 51–120 in Röhrig, E. & Ulrich, B. (Eds) Temperate Deciduous Forests. Ecosystems of the World. Amsterdam, The Netherlands, Elsevier.Google Scholar
Schaefer, M. (1992) Brohmer – Fauna von Deutschland. Heidelberg, Germany, Quelle & Meyer.Google Scholar
Scheu, S. (2002) The soil food web: structure and perspectives. European Journal of Soil Biology 38, 1120.CrossRefGoogle Scholar
Scheu, S. & Falca, M. (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia 123, 285296.Google Scholar
Scheu, S. & Setälä, H. (2002) Multitrophic interactions in decomposer food webs. pp. 223264in Tscharntke, T. & Hawkins, B.A. (Eds) Multitrophic Level Interactions. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Schimel, J.P. & Hättenschwiler, S. (2007) Nitrogen transfer between decomposing leaves of different N status. Soil Biology and Biochemistry 39, 14281436.CrossRefGoogle Scholar
Schmidt, O., Scrimgeour, C.M. & Handley, L.L. (1997) Natural abundance of 15N and 13C in earthworms from a wheat and a wheat-clover field. Soil Biology and Biochemistry 29, 13011308.Google Scholar
Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E. & Scrimgeour, C.M. (2004) Dual stable isotope analysis (d13C and d15N) of soil invertebrates and their food sources. Pedobiologia 48, 171180.Google Scholar
Steele, K.W. & Daniel, R.M. (1978) Fractionation of nitrogen isotopes by animals: a further complication to the use of variations in the natural abundance of 15N for tracer studies. Journal of Agricultural Science 90, 79.Google Scholar
Striganova, B.R. (1967) Über die Zersetzung von überwinterter Laubstreu durch Tausendfüßer und Landasseln. Pedobiologia 7, 125138.Google Scholar
Sunderland, K.D. (1975) The diet of some predatory arthropods in cereal crops. Journal of Applied Ecology 12, 507515.Google Scholar
Sunderland, K.D., Crook, N.E., Stacey, D.L. & Fuller, B.J. (1987) A study of feeding by polyphagous predators on cereal aphids using ELISA and gut dissection. Journal of Applied Ecology 24, 907933.Google Scholar
Swift, M.F., Heal, O.W. & Anderson, J.M. (1979) Decomposition in terrestrial ecosystems. Berkeley, California, USA, University of California Press.CrossRefGoogle Scholar
Tayasu, I. (1998) Use of carbon and nitrogen isotope ratios in termite research. Ecological Research 13, 377387.Google Scholar
Tayasu, I., Abe, T., Eggleton, P. & Bignell, D.E. (1997) Nitrogen and carbon isotope ratios in termites – an indicator of trophic habit along the gradient from wood-feeding to soil-feeding. Ecological Entomology 22, 343351.CrossRefGoogle Scholar
Vanderklift, M.A. & Ponsard, S. (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169182.CrossRefGoogle ScholarPubMed
Verhoef, H.A., Prast, J.E. & Verweij, R.A. (1988) Relative importance of fungi and algae in the diet and nitrogen nutrition of Orchesella cincta (L.) and Tomocerus minor (Lubbock) (Collembola). Functional Ecology 2, 195201.Google Scholar
Wachmann, E., Platen, R. & Barndt, D. (1995) Laufkäfer: Beobachtung und Lebensweise. Augsburg, Germany, Naturbuch-Verlag.Google Scholar
Wallwork, J.A. (1976) The Distribution and Diversity of Soil Fauna. London, UK, Academic Press.Google Scholar
Wedin, D.A., Tieszen, L.L., Dewey, B. & Pastor, J. (1995) Carbon isotope dynamics during grass decomposition and soil organic matter formation. Ecology 76, 13831392.CrossRefGoogle Scholar
Werner, M.R. & Dindal, D.L. (1987) Nutritional Ecology of soil arthropods. In: Nutritional ecology of insects, mites, spiders and related invertebrates. pp. 815836in Slansky, F. & Rodriguez, J.G. (Eds) Nutritional Ecology of Insects, Mites, and Spiders. New York, USA, J. Wiley.Google Scholar
Witt, R. (1998) Wespen – beobachten, bestimmen. Augsburg, Germany, Naturbuch-Verlag.Google Scholar
Wolters, V. (1985) Untersuchung zur Habitatbindung und Nahrungsbiologie der Springschwänze (Collembola) eines Laubwaldes unter besonderer Berücksichtigung ihrer Funktion in der Zersetzerkette. PhD dissertation, University of Göttingen, Göttingen, Germany.Google Scholar
Yoneyama, T., Handley, L.L., Scrimgeour, C.M., Fisher, D.B. & Raven, J.A. (1997) Variations of the natural abundances of nitrogen and carbon isotopes in Triticum aestivum, with special reference to phloem and xylem exudates. New Phytologist 137, 205213.CrossRefGoogle ScholarPubMed
Zachariae, G. (1963) Was leisten Collembolen für den Waldhumus? pp. 109124in Doeksen, J. & van der Drift, J. (Eds). Proceedings of the Colloquium on Soil Fauna, Soil Microflora and their Relationships. Amsterdam, The Netherlands, North-Holland Publishing Company.Google Scholar
Zahradnik, J. (1985) Käfer Mittel- und Nordwesteuropas. Hamburg, Germany, Paul Parey.Google Scholar
Zettel, J., Zettel, U., Suter, C., Streich, S. & Egger, B. (2002) Winter feeding behaviour of Ceratophysella sigillata (Collembola: Hypogastruridae) and the significance of eversible vesicles for resource utilisation. Pedobiologia 46, 404413.Google Scholar
Zheng, D.W., Bengtsson, J. & Agren, G.I. (1997) Soil food webs and ecosystem processes-decomposition in donor-control and Lotka-Volterra systems. American Naturalist 149, 125148.CrossRefGoogle Scholar
Zimmermann, M. & Spence, J.R. (1989) Prey use of the fishing spider Dolomedes triton (Pisauridae, Araneae): An important predator of the neuston community. Oecologia 80, 187194.CrossRefGoogle ScholarPubMed