Abstract
Knowledge of the interactions between organisms within trophic groups is important for an understanding of the role of biodiversity in ecosystem functioning. We hypothesised that interactions between bacterivorous nematodes of different life history strategies would affect nematode population development, bacterial community composition and activity, resulting in increased N mineralization. A microcosm experiment was conducted using three nematode species (Bursilla monhystera, Acrobeloides nanus and Plectus parvus). All the nematode species interacted with each other, but the nature and effects of these interactions depended on the specific species combination. The interaction between B. monhystera and A. nanus was asymmetrically competitive (0,−), whereas that between B. monhystera and P. parvus, and also A. nanus and P. parvus was contramensal (+, −). The interaction that affected microcosm properties the most was the interaction between B. monhystera and P. parvus. This interaction affected the bacterial community composition, increased the bacterial biomass and increased soil N mineralization. B. monhystera and P. parvus have the most different life history strategies, whereas A. nanus has a life history strategy intermediate to those of B. monhystera and P. parvus. We suggest that the difference in life history strategies between species of the same trophic group is of importance for their communal effect on soil ecosystem processes. Our results support the idiosyncrasy hypothesis on the role of biodiversity in ecosystem functioning.
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References
Anderson RV, Coleman DC (1981) Population development and interactions between two species of bacteriophagic nematodes. Nematologica 27:6–19
Anderson RV, Coleman DC (1982) Nematode temperature responses: a niche dimension in populations of bacterial-feeding nematodes. J Nematol 14:69–76
Anderson RV, Gould WD, Woods LE, Cambardella C, Ingham RE, Coleman DC (1983) Organic and inorganic nitrogenous losses by microbivorous nematodes in soil. Oikos 40:75–80
Arthur W (1986) On the complexity of a simple environment: competition, resource partitioning and facilitation in a two-species Drosophila system. Philos Trans R Soc Lond Ser B 313:471–508
Bååth E, Lohm U, Lundgren B, Rosswall T, Söderström B, Sohlenius B (1981) Impact of microbial feeding animals on total soil activity and nitrogen dynamics: a soil microcosm experiment. Oikos 37:257–264
Ballinger SJ, Head IM, Curtis TP, Godley AR (2002) The effect of C/N ratio on ammonia oxidising bacteria community structure in a laboratory nitrification-denitrification reactor. Water Sci Technol 46:543–550
Bardgett RD, Cook R (1998) Functional aspects of soil animal diversity in agricultural grasslands. Appl Soil Ecol 10:263–276
Bardgett RD, Keiller S, Cook R, Gilburn AS (1998) Dynamic interactions between soil animals and microorganisms in upland grassland soils amended with sheep dung: a microcosm experiment. Soil Biol Biochem 30:531–539
Bardgett RD, Cook R, Yeates GW, Denton CS (1999) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33
Begon M, Harper JL, Townsend CR (1990) Ecology: individuals, populations and communities, 2nd edn. Blackwell , Boston, Mass.
Bloem J, Breure AM (2003) Microbial indicators. In: Markert BA, Breure AM, Zechmeister HG (eds) Bioindicators/biomonitors—principles, assessment, concepts. Elsevier, Amsterdam, pp 259–282
Bloem J, Bolhuis PR, Veninga M, Wieringa J (1995a) Microscopic methods for counting bacteria and fungi in soil. In: Alef KPN (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 162–173
Bloem J, Veninga M, Shepherd J (1995b) Fully automatic determination of soil bacterium numbers, cell volumes and frequencies of dividing cells by confocal laser scanning microscopy and image analysis. Appl Environ Microbiol 61:926–936
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19
Bouwman LA, Hoenderboom GHJ, Van der Maas KJ, De Ruiter PC (1996) Effects of nematophagous fungi on numbers and death rates of bacterivorous nematodes in arable soil. J Nematol 28:26–35
Brussaard L (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570
Brussaard L, Noordhuis R, Geurs M, Bouwman LA (1995) Nitrogen mineralization in soil in microcosms with or without bacterivorous nematodes and nematophagous mites. Acta Zool Fenn 196:15–21
Cragg RG, Bardgett RD (2001) How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081
De Mesel I, Derycke S, Swings J, Vincx M, Moens T (2003) Influence of bacterivorous nematodes on the decomposition of cordgrass. J Exp Mar Biol Ecol 296:227–242
Didden WAM et al (1993) Soil meso-and macrofauna in two agricultural systems: factors affecting population dynamics and evaluation of their role in carbon and nitrogen dynamics. Agric Ecosyst Environ 51:171–186
Dilly O, Bloem J, Vos A, Munch JC (2004) Bacterial diversity during litter decomposition in agricultural soils. Appl Environ Microbiol 70:468–474
Djigal D, Brauman A, Diop TA, Chotte JL, Villenave C (2004) Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth. Soil Biol Biochem 36:323–331
Faber JH (1991) Functional classification of soil fauna: a new approach. Oikos 62:110–117
Faber JH, Verhoef HA (1991) Functional differences between closely related soil arthropods with respect to decomposition and nitrogen mobilization in a pine forest. Soil Biol Biochem 23:15–23
Ferris H, Matute MM (2003) Structural and functional succession in the nematode fauna of a soil food web. Appl Soil Ecol 23:93–110
Ferris H, Venette RC, Van der Meulen HR, Lau SS (1998) Nitrogen mineralization by bacterial feeding nematodes: verification and measurement. Plant Soil 203:159–171
Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195–217
Griffiths BS (1994) Microbial-feeding nematodes and Protozoa in soil: their effects on microbial activity and nitrogen mineralization in decomposition hotspots and the rhizosphere. Plant Soil 164:25–33
Griffiths BS, Bonkowski M, Dobson F, Caul S (1999) Changes in soil microbial community structure in the presence of microbial-feeding nematodes and Protozoa. Pedobiologia 43:297–304
Heemsbergen DA, Berg MP, Loreau M, Van Hal JR, Faber JH, Verhoef HA (2004) Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science (in press)
Huhta V, Viberg K (1999) Competitive interaction between the earthworm Dendrobaena octaedra and the enchytraeid Cognettia sphagnetorum. Pedobiologia 43:886–890
Ingham RE, Trofymore JA, Ingham ER, Coleman DC (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55:119–140
Laakso J, Setälä H (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87:57–64
Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461
Michel PH, Bloem J (1993) Conversion factors for estimation of cell production rates of soil bacteria from thymidine and leucine incorporation. Soil Biol Biochem 25:943–950
Mikola J, Setälä H (1998a) No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153–164
Mikola J, Setälä H (1998b) Productivity and trophic-level biomasses in a microbial-based soil food web. Oikos 82:158–168
Mikola J, Setälä H (1998c) Relating species diversity to ecosystem functioning: mechanistic backgrounds and experimental approach with a decomposer food web. Oikos 83:180–194
Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM (1995) Empirical evidence that declining species diversity may alter the performance of terrestrial ecosystems. Philos Trans R Soc Lond Ser B 347:249–262
Oostenbrink M (1960) Estimating nematode populations by some selected methods. In: Sasser JM, Jenkins WR (eds) Nematology. University of North Carolina Press, Chapel Hill, N.C., pp 85–102
Sonneman I, Dogan H, Klein A, Pieper B, Ekschmitt K, Wolters V (1999) Response of soil microflora to changes in nematode abundance—evidence for large scale effects in grassland soil. J Plant Nutr Soil Sci 162:385–391
Theenhaus A, Scheu A, Schaeffer M (1999) Contramensal interactions between two collembolan species: effects on populations development and soil processes. Funct Ecol 13:238–246
Van Elsas JD, Smalla K (1995) Extraction of microbial community DNA from soils. In: Akkermans ADL, Van Elsas JD, De Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer , Dordrecht, section 1.3.3.1–1.3.3.11
Verhoef HA, Brussaard L (1990) Decomposition and nitrogen mineralization in natural and agro ecosystems: the contribution of soil animals. Biogeochem 11:175–211
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Oxford
Acknowledgements
We are grateful to An Vos for analyses of the bacterial community, Jan Kammenga and Martijs Jonker for providing the nematode species P. parvus and instructions for culturing nematodes, Jaap Nelemans and Willeke van Tintelen for assistance in the laboratory and Claire Boddington for checking the English. This study was funded by the Stimulation Programme Biodiversity of the NWO, the Netherlands Organisation for Scientific Research. J. Bloem and J. H. Faber were supported by the Dutch Ministry of Agriculture, Nature and Food Quality through the DWK program 352 on Agrobiodiversity.
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Postma-Blaauw, M.B., de Vries, F.T., de Goede, R.G.M. et al. Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142, 428–439 (2005). https://doi.org/10.1007/s00442-004-1741-x
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DOI: https://doi.org/10.1007/s00442-004-1741-x