Biology Bulletin Reviews

, Volume 4, Issue 5, pp 393–403 | Cite as

Trophic chains in the soil

Article

Abstract

The trophic links of soil animals are extensively diverse but also flexible. Moreover, the feeding activity of large soil saprotrophs often cascades into a range of ecosystem-level consequences via the ecological engineering. An improved knowledge of the main sources of energy utilized by soil animals is needed for understanding the functional structure of soil animal communities and their participation in the global carbon cycling. Using published and original data, we consider the relative importance of dead organic matter and saprotrophic microorganisms as a basal energy source in the detritus-based food chains, the feeding of endogeic macrofauna on the stabilized soil organic matter, and the role of recent photosynthate in the energy budget of soil communities. Soil food webs are spatially and functionally compartmentalized, though the separation of food chains into bacteriaand fungi-based channels seems to be an oversimplification. The regulation of litter decomposition rates via top-down trophic interactions across more than one trophic level is only partly supported by experimental data, but mobile litter-dwelling predators play a crucial role in integrating local food webs within and across neighboring ecosystems.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amelung, W., Brodowski, S., Sandhage-Hofmann, A., and Bol, R., Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter, Adv. Agron., 2008, vol. 100, pp. 155–250.Google Scholar
  2. Anderson, J.M., The enigma of soil animal species diversity, in Progress in Soil Zoology, Vanek, J., Ed., Prague: Academia, 1975, pp. 51–58.Google Scholar
  3. Andren, O., Brussaard, L., and Clarholm, M., Soil organism influence on ecosystem-level processes — bypassing the ecological hierarchy? Appl. Soil Ecol., 1999, vol. 11, pp. 177–188.Google Scholar
  4. Ballinger, A. and Lake, P.S., Energy and nutrient fluxes from rivers and streams into terrestrial food webs, Mar. Freshwater Res., 2006, vol. 57, pp. 15–28.Google Scholar
  5. Barois, I. and Lavelle, P., Changes in respiration rate and some physicochemical properties of a tropical soil during transit through Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta), Soil Biol. Biochem., 1986, vol. 18, pp. 539–541.Google Scholar
  6. Baylis, I.P., Cherrett, I.M., and Ford, I.B., A survey of the invertebrates feeding on living clover roots (Trifolium repens L.) using 32P as a radiotracer, Pedobiologia, 1986, vol. 29, pp. 201–208.Google Scholar
  7. Begon, M., Harper, J.L., and Townsend, C.R., Ecology: Individuals, Populations, and Communities, Blackwell Sci., 1996.Google Scholar
  8. Beklemishev, V.N., Classification of biocenotic (simphysiological) relationships, Byull. Mosk. O-va. Ispyt. Prir., Otd. Biol., 1951, no. 56, pp. 3–30.Google Scholar
  9. Berg, M.P. and Bengtsson, J., Temporal and spatial variability in soil food web structure, Oikos, 2007, vol. 116, pp. 1789–1804.Google Scholar
  10. Berg, M., de Ruiter, P., Didden, W., Janssen, M., Schouten, T., and Verhoef, H., Community food web, decomposition and nitrogen mineralization in a stratified Scots pine forest soil, Oikos, 2001, vol. 94, pp. 130–142.Google Scholar
  11. Bocock, K.L. and Gilbert, O.J.W., The disappearance of leaf litter under different woodland conditions, Plant Soil, 1957, vol. 9, pp. 179–185.Google Scholar
  12. Bohlen, P.J., Scheu, S., Hale, C.M., McLean, M.A., Migge, S., Groffman, P.M., and Parkinson, D., Nonnative invasive earthworms as agents of change in northern temperate forests, Front. Ecol. Environ., 2004, vol. 2, pp. 427–435.Google Scholar
  13. Bonkowski, M., Villenave, C., and Griffiths, B., Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots, Plant Soil, 2009. V 321, pp. 213–233.Google Scholar
  14. Briones, M.J.I., Garnett, M.H., and Piearce, T.G., Earthworm ecological groupings based on 14C analysis, Soil Biol. Biochem., 2005, vol. 37, pp. 2145–2149.Google Scholar
  15. Briones, M.J.I. and Ineson, P., Use of 14C carbon dating to determine feeding behavior of enchytraeids, Soil Biol. Biochem., 2002, vol. 34, pp. 881–884.Google Scholar
  16. Brown, G.G., Barois, I., and Lavelle, P., Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains, Eur. J. Soil Biol., 2000, vol. 36, pp. 177–198.Google Scholar
  17. Cortez, J. and Bouche, M.B., Do earthworms eat living roots, Soil Biol. Biochem., 1992, vol. 24, pp. 913–915.Google Scholar
  18. Crotty, F.V., Blackshaw, R.P., and Murray, P.J., Tracking the flow of bacterially derived 13C and 15N through soil faunal feeding channels, Rapid Commun. Mass Spectrom., 2011, vol. 25, pp. 1503–1513.PubMedGoogle Scholar
  19. Daufresne, T. and Loreau, M., Ecological stoichiometry, primary producer-decomposer interactions, and ecosystem persistence, Ecology, 2001, vol. 82, pp. 30693082.Google Scholar
  20. Dreyer, J., Hoekman, D., and Gratton, C., Lake-derived midges increase abundance of shoreline terrestrial arthropods via multiple trophic pathways, Oikos, 2012, vol. 121, pp. 252–258.Google Scholar
  21. Ettema, C.H. and Wardle, D.A., Spatial soil ecology, Trends Ecol. Evol., 2002, vol. 17, pp. 177–183.Google Scholar
  22. Frelich, L.E., Hale, C.M., Scheu, S., Holdsworth, A.R., Heneghan, L., Bohlen, P.J., and Reich, P.B., Earthworm invasion into previously earthworm-free temperate and boreal forests, Biol. Invasions, 2006, vol. 8, pp. 1235–1245.Google Scholar
  23. Gange, A., Arbuscular mycorrhizal fungi, Collembola and plant growth, Trends Ecol. Evol., 2000, vol. 15, pp. 369–372.PubMedGoogle Scholar
  24. Geffen, K.G., van Berg, M.P., and Aerts, R., Potential macro-detritivore range expansion into the subarctic stimulates litter decomposition: a new positive feedback mechanism to climate change? Oecologia, 2011, vol. 167, pp. 1163–1175.PubMedPubMedCentralGoogle Scholar
  25. Ghilarov, M.S., The key identification factors of soil parasites and their significance for rubber-bearing cultures, Zashch. Rast., 1937, no. 13, pp. 41–53.Google Scholar
  26. Ghilarov, M.S., Soil fauna and soil life, Pochvovedenie, 1939, no. 6, pp. 3–15.Google Scholar
  27. Ghilarov, M.S., Ratio of dimensions and number of soil invertebrates, Dokl. Akad. Nauk, 1944, no. 43, pp. 283–285.Google Scholar
  28. Ghilarov, M.S., On the interrelations between soil dwelling invertebrates and soil microorganisms, in Soil Organisms, Doeksen, J. and van der Drift, J., Eds., Amsterdam, 1963, pp. 255–259.Google Scholar
  29. Ghilarov, M.S., Soil layer of land biocenosises, Usp. Sovrem. Biol., 1968, vol. 66, pp. 121–135.Google Scholar
  30. Ghilarov, M.S., Some general statements on ecology of terrestrial invertebrates, Zh. Obshch. Biol., 1973, vol. 34, pp. 795–806.Google Scholar
  31. Ghilarov, M.S. and Chernov, Yu.I., Soil invertebrates in community composition of moderate climate zone, in Resursy biosfery (Biosphere Resources), Leningrad: Nauka, 1975, pp. 218–240.Google Scholar
  32. Gladyshev, M.I., Arts, M.T., and Sushchik, N.N., Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems, in Lipids in Aquatic Ecosystems, Arts, M.T., Brett, M.T., and Kainz, M.J. Eds., New York: Springer, 2009, pp. 179–209.Google Scholar
  33. Goncharov, A.A., Kuznetsov, A.I., D’yakov, L.M., and Tiunov, A.V., Trophic links of soil arthropods and aquatic ecosystems of Omsk Nature Reserve (according to isotope data analysis), Izv. Penz. Gos. Pedagog. Univ. im V.G. Belinskogo, 2011, no. 25, pp. 337–344.Google Scholar
  34. Gratton, C., Donaldson, J., and van der Zanden, M.J., Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland, Ecosystems, 2008, vol. 11, pp. 764–774.Google Scholar
  35. Gunn, A. and Cherrett, J.M., The exploitation of food resources by soil meso- and macroinvertebrates, Pedobiologia, 1993, vol. 37, pp. 303–327.Google Scholar
  36. Halaj, J. and Wise, D.H., Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web, Ecology, 2002, vol. 83, pp. 3141–3151.Google Scholar
  37. Hassall, M., Adl, S., Berg, M., Griffiths, B., and Scheu, S., Soil fauna-microbe interactions: towards a conceptual framework for research, Eur. J. Soil Biol., 2006, vol. 42, pp. 54–60.Google Scholar
  38. Hattenschwiler, S., Tiunov, A.V., and Scheu, S., Biodiversity and litter decomposition in terrestrial ecosystems, Annu. Rev. Ecol. Syst., 2005, vol. 36, pp. 191–218.Google Scholar
  39. Hawlena, D., Strickland, M.S., Bradford, M.A., and Schmitz, O.J., Fear of predation slows plant-litter decomposition, Science, 2012, vol. 336, pp. 1434–1438.PubMedGoogle Scholar
  40. Hedlund, K. and Sjogren Ohrn, M., Tritrophic interactions in a soil community enhance decomposition rates, Oikos, 2000, vol. 88, pp. 585–591.Google Scholar
  41. Hendrix, P.F., Callaham, M.A., Drake, J.M., Huang, C.Y., James, S.W., Snyder, B.A., and Zhang, W.X., Pandora’s box contained bait: The global problem of introduced earthworms, Annu. Rev. Ecol. Syst., 2008, vol. 39, pp. 593–613.Google Scholar
  42. Hunt, H.W., Coleman, D.C., Ingham, E.R., Ingham, R.E., Elliott, E.T., Moore, J.C., Rose, S.L., Reid, C.P.P., and Morley, C.R., The detrital food web in a shortgrass prairie, Biol. Fertil. Soils, 1987, vol. 3, pp. 57–68.Google Scholar
  43. Hyodo, F., Tayasu, I., Konate, S., Tondoh, J.E., Lavelle, P., and Wada, E., Gradual enrichment of 15N with humification of diets in a below-ground food web: relationship between 15N and diet age determined using 14C, Funct. Ecol., 2008, vol. 22, pp. 516–522.Google Scholar
  44. Hyodo, F., Tayasu, I., and Wada, E., Estimation of the longevity of C in terrestrial detrital food webs using radiocarbon (14C): how old are diets in termites? Funct. Ecol., 2006, vol. 20, pp. 385–393.Google Scholar
  45. Kajak, A., The role of soil predators in decomposition process, Eur. J. Entomol., 1995, vol. 92, pp. 573–780.Google Scholar
  46. Kampichler, C. and Bruckner, A., The role of microarthropods in terrestrial decomposition: a meta-analysis of 40 years of litterbag studies, Biol. Rev., 2009, vol. 84, pp. 375–389.PubMedGoogle Scholar
  47. Kemmitt, S.J., Lanyon, C.V., Waite, I.S., Wen, Q., Addiscott, T.M., Bird, N.R.A., O’Donnell, A.G., and Brookes, P.C., Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass — a new perspective, Soil Biol. Biochem., 2008, vol. 40, pp. 61–73.Google Scholar
  48. Kleber, M., What is recalcitrant soil organic matter? Environ. Chem., 2010, vol. 7, pp. 320–332.Google Scholar
  49. Kurcheva, G.F., Rol’ pochvennykh zhivotnykh v razlozhenii i gumifikatsii rastitel’nykh ostatkov (Role of Soil Fauna in Decomposition and Humification of the Plant Litter), Moscow: Nauka, 1971.Google Scholar
  50. Kuzyakov, Ya.V., Isotope-marker analysis of air carbon translocation by the plants to the soil (literature survey), Pochvovedenie, 2001, no. 1, pp. 36–51.Google Scholar
  51. Kuzyakov, Y., Friedel, J.K., and Stahr, K., Review of mechanisms and quantification of priming effects, Soil Biol. Biochem., 2000, vol. 32, pp. 1485–1498.Google Scholar
  52. Laakso, J. and Setala, H., Population- and ecosystem-level effects of predation on microbial-feeding nematodes, Oecologia, 1999, vol. 120, pp. 279–286.Google Scholar
  53. Lavelle, P. and Gilot, C., Priming effects of macroorganisms on microflora: A key process of soil function? in Beyond the Biomass, Ritz, K., Dighton, J., and Giller, K.E., Eds., New York: Wiley, 1994, pp. 173–180.Google Scholar
  54. Lindahl, B.O., Taylor, A.F.S., and Finlay, R.D., Defining nutritional constraints on carbon cycling in boreal forests — towards a less “phytocentric” perspective, Plant Soil, 2002, vol. 242, pp. 123–135.Google Scholar
  55. Lukesova, A. and Frouz, J., Soil and freshwater microalgae as a food source for invertebrates in extreme environments, in Algae and Cyanobacteria in Extreme Environments, Seckbach, J., Ed., 2007, pp. 265–284.Google Scholar
  56. Maraun, M., Erdmann, G., Fischer, B.M., Pollierer, M.M., Norton, R.A., Schneider, K., and Scheu, S., Stable isotopes revisited: Their use and limits for oribatid mite trophic ecology, Soil Biol. Biochem., 2011, vol. 43, pp. 877–882.Google Scholar
  57. Martin, A., Cortez, J., Barois, I., and Lavelle, P., The production of intestinal mucus by earthworms: a key process in their interactions with the soil microflora, Rev. d’Ecol. Biol. Sol, 1987, vol. 24, pp. 549–558.Google Scholar
  58. Martin, A., Mariotti, A., Balesdent, J., and Lavelle, P., Soil organic matter assimilation by a geophagous tropical earthworm based on 13C measurements, Ecology, 1992, vol. 73, pp. 118–128.Google Scholar
  59. McGlynn, T.P. and Poirson, E.K., Ants accelerate litter decomposition in a Costa Rican lowland tropical rain forest, J. Trop. Ecol., 2012, vol. 28, pp. 437–443.Google Scholar
  60. Migge-Kleian, S., McLean, M.A., Maerz, J.C., and Heneghan, L., The influence of invasive earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms, Biol. Invasions, 2006, vol. 8, pp. 1275–1285.Google Scholar
  61. Mikola, J., Bardgett, R.D., and Hedlund, K., Biodiversity, ecosystem functioning and soil decomposer food webs, in Biodiversity and Ecosystem Functioning: Synthesis and Perspectives, Loreau, M., Naeem, S., and Inchausti, P., Eds., Oxford: Oxford Univ. Press, 2002, pp. 169–180.Google Scholar
  62. Mikola, J. and Setala, H., No evidence of trophic cascades in an experimental microbial-based food web, Ecology, 1998, vol. 79, pp. 153–164.Google Scholar
  63. Moore, J.C., Berlow, E.L., Coleman, D.C., de Ruiter, P.C., Dong, Q., Hastings, A., Johnson, N.C., McCann, K.S., Melville, K., Morin, P.J., Nadelhoffer, K., Rosemond, A.D., Post, D.M., Sabo, J.L., Scow, K.M., Vanni, M.J., and Wall, D.H., Detritus, trophic dynamics and biodiversity, Ecol. Lett., 2004, vol. 7, pp. 584–600.Google Scholar
  64. Moore, J.C. and de Ruiter, P.C., Compartmentalization of resource utilization within soil ecosystems, in Multitrophic Interactions in Terrestrial Systems, Gange, A.C. and Brown, V.K., Eds., Oxford: Blackwell Sci., 1997, pp. 375–393.Google Scholar
  65. Morris, S.J., Spatial distribution of fungal and bacterial biomass in southern Ohio hardwood forest soils: fine scale variability and microscale patterns, Soil Biol. Biochem., 1999, vol. 31, pp. 1375–1386.Google Scholar
  66. Ostle, N., Briones, M.J.I., Ineson, P., Cole, L., Staddon, P., and Sleep, D., Isotopic detection of recent photosynthate carbon flow into grassland rhizosphere fauna, Soil Biol. Biochem., 2007, vol. 39, pp. 768–777.Google Scholar
  67. Paetzold, A., Lee, M., and Post, D.M., Marine resource flows to terrestrial arthropod predators on a temperate island: the role of subsidies between systems of similar productivity, Oecologia, 2008, vol. 157, pp. 653–659.PubMedGoogle Scholar
  68. Paetzold, A., Schubert, C.J., and Tockner, K., Aquatic terrestrial linkages along a braided-river: Riparian arthropods feeding on aquatic insects, Ecosystems, 2005, vol. 8, pp. 748–759.Google Scholar
  69. Perel’, T.S., Living forms of Lumbricidae, Zh. Obshch. Biol., 1975, vol. 36, pp. 189–202.PubMedGoogle Scholar
  70. Persson, T. and Lohm, U., Energetical significance of the annelids and arthropods in a Swedish grassland soil, Ecol. Bull. (Stockholm), 1977, vol. 23, pp. 1–211.Google Scholar
  71. Petersen, H. and Luxton, M.A., A comparative analysis of soil fauna populations and their role in decomposition processes, Oikos, 1982, vol. 39, pp. 287–388.Google Scholar
  72. Pimm, S.L., Food Webs, London: Chapman and Hall, 1982.Google Scholar
  73. Pokarzhevskii, A.D., Gongal’skii, K.B., Zaitsev, A.S., and Savin, F.A., Prostranstvennaya ekologiya pochvennykh zhivotnykh (Spatial Ecology of Soil Fauna), Moscow: KMK, 2007.Google Scholar
  74. Pokarzhevskii A.D., van Straalen N.M., Zaboev D.P., Zaitsev A.S. Microbial links and element flows in nested detrital food-webs, Pedobiologia, 2003, vol. 47, pp. 213–224.Google Scholar
  75. Polis, G.A., Anderson, W.B., and Holt, R.D., Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs, Annu. Rev. Ecol., Evol., Syst., 1997, vol. 28, pp. 289–316.Google Scholar
  76. Pollierer, M.M., Dyckmans, J., Scheu, S., and Haubert, D., Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound specific 13C fatty acid analysis, Funct. Ecol., 2012, vol. 26, pp. 978–990.Google Scholar
  77. Pollierer, M.M., Langel, R., Korner, C., Maraun, M., and Scheu, S., The underestimated importance of belowground carbon input for forest soil animal food webs, Ecol. Lett., 2007, vol. 10, pp. 729–736.PubMedGoogle Scholar
  78. Pollierer, M.M., Langel, R., Scheu, S., and Maraun, M., Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C), Soil Biol. Biochem., 2009, vol. 41, pp. 1221–1226.Google Scholar
  79. Powers, J.S., Montgomery, R.A., Adair, E.C., Brearley, F.Q., Dewalt, S.J., Castanho, C.T., Chave, J., Deinert, E., Ganzhorn, J.U., Gilbert, M.E., Gonzalez-Iturbe, J.A., Bunyavejchewin, S., Grau, H.R., Harms, K.E., Hiremath, A., Iriarte-Vivar, S., Manzane, E., de Oliveira, A.A., Poorter, L., Ramanamanjato, J.B., Salk, C., Varela, A., Weiblen, G.D., and Lerdau, M.T., Decomposition in tropical forests: a pan-tropical study of the effects of litter type, litter placement and mesofaunal exclusion across a precipitation gradient, J. Ecol., 2009, vol. 97, pp. 801–811.Google Scholar
  80. Power, M.E. and Rainey, W.E., Food webs and resource sheds: towards spatially delimiting trophic interactions, in The Ecological Consequences of Environmental Heterogeneity, Hutchings, M.J., John, E.A., and Stewart, A.J.A., Eds., Oxford: Blackwell Sci., 2000, pp. 291–314.Google Scholar
  81. Prescott, C.E., Do rates of litter decomposition tell us anything we really need to know? For. Ecol. Manage., 2005, vol. 220, pp. 66–74.Google Scholar
  82. Prescott, C.E., Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry, 2010, vol. 101, pp. 133–149.Google Scholar
  83. Putten, W.H. van der Bardgett, R.D., de Ruiter, P.C., Hol, W.H.G., Meyer, K.M., Bezemer, T.M., Bradford, M.A., Christensen, S., Eppinga, M.B., Fukami, T., Hemerik, L., Molofsky, J., Schadler, M., Scherber, C., Strauss, S.Y., Vos, M., and Wardle, D.A., Empirical and theoretical challenges in aboveground-belowground ecology, Oecologia, 2009, vol. 161, pp. 1–14.PubMedPubMedCentralGoogle Scholar
  84. Remen, C., Persson, T., Finlay, R., and Ahlstrom, K., Responses of oribatid mites to tree girdling and nutrient addition in boreal coniferous forests, Soil Biol. Biochem., 2008, vol. 40, pp. 2881–2890.Google Scholar
  85. Rooney, N., McCann, K., Gellner, G., and Moore, J.C., Structural asymmetry and the stability of diverse food webs, Nature, 2006, vol. 442, pp. 265–269.PubMedGoogle Scholar
  86. Saetre, P. and Baath, E., Spatial variation and patterns of soil microbial community structure in a mixed sprucebirch stand, Soil Biol. Biochem., 2000, vol. 32, pp. 909–917.Google Scholar
  87. Sazonova, O.N., Outflow of organic matter by mosquito in relief declivity to plakor, in Mater. soveshch. “Sredoobrazuyushchaya deyatel’nost’ zhivotnykh,” 17–18 dekabrya 1970 g. (Proc. Meeting “Environment-Forming Activity of Animals,” December 17–18, 1970), Moscow: Mosk. Gos. Univ., 1970, pp. 65–71.Google Scholar
  88. Scheu, S., Plants and generalist predators as links between the below-ground and above-ground system, Basic Appl. Ecol., 2001, vol. 2, pp. 3–13.Google Scholar
  89. Scheu, S. and Falca, M., 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, 2000, vol. 123, pp. 285–296.Google Scholar
  90. Scheu, S. and Schaefer, M., Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources, Ecology, 1998, vol. 79, no. 5, pp. 1573–1585.Google Scholar
  91. Scheunemann, N., Scheu, S., and Butenschoen, O., Incorporation of decade old soil carbon into the soil animal food web of an arable system, Appl. Soil Ecol., 2010, vol. 46, pp. 59–63.Google Scholar
  92. Schmidt, M.W.I., Torn, M.S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I.A., Kleber, M., Kogel-Knabner, I., Lehmann, J., Manning, D.A.C., Nannipieri, P., Rasse, D.P., Weiner, S., and Trumbore, S.E., Persistence of soil organic matter as an ecosystem property, Nature, 2011, vol. 478, pp. 49–56.PubMedGoogle Scholar
  93. Shilenkova, O.L. and Tiunov, A.V., Influence of free carbon on abundance of collembolan and destruction rate of litter: laboratory experiment, Izv. Penz. Gos. Pedagog. Univ. im V.G. Belinskogo, 2011, no. 25, pp. 478–483.Google Scholar
  94. Shtina, E.A., Interaction of soil algae and invertebrates, in Razlozhenie rastitel’nykh ostatkov v pochve (Litter Decomposition in Soil), Moscow: Nauka, 1985, pp. 90–104.Google Scholar
  95. Shurin, J.B., Gruner, D.S., and Hillebrand, H., All wet or dried up? Real differences between aquatic and terrestrial food webs, Proc. R. Soc. B, 2006, vol. 273, pp. 1–9.PubMedPubMedCentralGoogle Scholar
  96. Soe, A.R.B. and Buchmann, N., Spatial and temporal variations in soil respiration in relation to stand structure and soil parameters in an unmanaged beech forest, Tree Physiol., 2005, vol. 25, pp. 1427–1436.PubMedGoogle Scholar
  97. Spain, A.V., Saffigna, P.G., and Wood, A.W., Tissue carbon source for Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) in a sugarcane ecosystem, Soil Biol. Biochem., 1990, vol. 22, pp. 703–706.Google Scholar
  98. Sterner, R.W. and Elser, J.J., Ecological Stoichiometry: The Biology of Elements from Molecules to Biosphere, Princeton: Princeton Univ. Press, 2002.Google Scholar
  99. Strickland, M.S., Wickings, K., and Bradford, M.A., The fate of glucose, a low molecular weight compound of root exudates, in the belowground foodweb of forests and pastures, Soil Biol. Biochem., 2012, vol. 49, pp. 23–29.Google Scholar
  100. Striganova, B.R., Pitanie pochvennykh saprofagov (Nutrition of Soil Saprophages), Moscow: Nauka, 1980.Google Scholar
  101. Striganova, B.R., Systemic analysis of biocenotic links in soil communities, in Chteniya pamyati akademika M.S. Gilyarova (Readings in the Memory of M.S. Ghilarov), Moscow: KMK, 2006, pp. 16–38.Google Scholar
  102. Swift, M.J., Heal, O.W., and Anderson, J.M., Decomposition in Terrestrial Ecosystems, Oxford: Blackwell, 1979.Google Scholar
  103. Tiunov, A.V., Mechanism of influence of the earthworms on other components of soil biota, in Chteniya pamyati akademika M.S. Gilyarova (Readings in the Memory of M.S. Ghilarov), Moscow: KMK, 2008, pp. 49–86.Google Scholar
  104. Trigo, D. and Lavelle, P., Changes in respiration rate and some physicochemical properties of soil during gut transit through Allolobophora molleri (Lumbricidae, Oligochaeta), Biol. Fertil. Soils, 1993, vol. 15, pp. 85–188.Google Scholar
  105. Tiunov, A.V. and Scheu, S., Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization, Oecologia, 2004, vol. 138, pp. 83–90.PubMedGoogle Scholar
  106. Visser, S., Role of soil invertebrates in determining the composition of soil microbial communities, in Ecological Interactions in Soil, Fitter, A.H., Atkinson, D., Read, D.J., and Usher, M.B., Eds., Oxford: Blackwell Sci., 1985, pp. 297–317.Google Scholar
  107. Wall, D.H., Bradford, M.A., John, M.G.S., Trofymow, J.A., et al., Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent, Global Change Biol., 2008, vol. 14, pp. 2661–2677.Google Scholar
  108. Wardle, D.A., Communities and ecosystems: linking the aboveground and belowground components. Princeton: Princeton Univ. Press, 2002.Google Scholar
  109. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., Putten, W.H., and van der Wall, D.H., Ecological linkages between aboveground and belowground biota, Science, 2004, vol. 304, pp. 1629–1633.PubMedGoogle Scholar
  110. Wardle, D.A., Karl, B.J., Beggs, J.R., Yeates, G.W., Williamson, W.M., and Bonner, K.I., Determining the impact of scale insect honeydew, and invasive wasps and rodents, on the decomposer subsystem in a New Zealand beech forest, Biol. Invasions, 2010, vol. 12, pp. 2619–2638.Google Scholar
  111. Wardle, D.A. and Yeates, G.W., The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer foodwebs, Oecologia, 1993, vol. 93, pp. 303–306.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia

Personalised recommendations