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Predator–prey interaction in soil food web: functional response, size-dependent foraging efficiency, and the influence of soil texture

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Abstract

In a series of laboratory experiments, we presented carnivorous Macrobiotus richtersi (Tardigrada, Macrobiotidae) with nematode prey to assess their importance as predator. We investigated consumption rate for (a) different prey densities (10–400 prey individuals), (b) different prey biomasses (22–80 ng), (c) different prey species (Pelodera teres, Rhabditidae, versus Acrobeloides nanus, Cephalobidae) and (d) different environments (2-D agar surface versus 3-D sand fractions of three different textures). M. richtersi consumed up to 4.6 μg nematode prey in 4 h, that is, 43% of the tardigrade’s body mass. Predation rate was positively correlated with prey density. The optimal prey in the present investigation was the biggest prey because it yielded the highest biomass uptake per time. In addition, the size of M. richtersi played an important role in consumption rate. Bacterivorous nematodes reacted differently to attack. Even in a water film on stiff agar where nematode agility was limited, a vigorous undulation reaction of P. teres led to a measurable reduction in consumption rate. A. nanus, in contrast, showed little response to attack. Microcosm experiments with sands of different particle size demonstrated that M. richtersi is able to chase and consume small bacterivorous nematodes in a 3-D soil matrix. However, consumption rate in sand microcosms was significantly reduced compared with pure agar. The sand matrix improved nematode agility and possibly provided small pores as refuge for the nematodes. The lowest consumption rate was observed in fine sand. Effects of predatory tardigrades on nematode numbers in the field are discussed.

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References

  • Anderson JM (1995) Soil organisms as engineers: microsite modulation of macroscale processes. In: Jones CG, Lawton JK (eds) Linking species and ecosystems. Chapman and Hall, New York, pp 94–106

    Google Scholar 

  • Andrássy I (1956) Die Rauminhalts- und Gewichtsbestimmung der Fadenwürmer (Nematoden). Acta Zool 2:1–15

    Google Scholar 

  • Beier S, Bolley M, Traunspurger W (2004) Predator–prey interactions between Dugesia gonocephala and free-living nematodes. Freshw Biol 49:77–86

    Google Scholar 

  • Bengtsson J, Wei Zheng D, Agren GI, Persson T (1995) Food webs in soil: an interface between population and ecosystem ecology. In: Jones CG, Lawton JK (eds) Linking species and ecosystems. Chapman and Hall, New York, pp 159–165

    Google Scholar 

  • Bilgrami AL (1992) Resistance and susceptibility of prey nematodes to predation and strike rate of the predators, Mononchus aquaticus, Dorylaimus stagnalis and Aquatides thornei. Fundam Appl Nematol 15:265–270

    Google Scholar 

  • Bilgrami AL (1993) Analysis of the predation by Aporcelaimellus nivalis on prey nematodes from different prey trophic categories. Nematologica 39:356–365

    Google Scholar 

  • 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

    Google Scholar 

  • Cogni R, Freitas AVL, Amaral Filho BF (2002) Influence of prey size on predation success by Zelus longipes L. (Het., Reduviidae). J Appl Entomol 126:74–78

    Google Scholar 

  • Coleman DC, Anderson RV, Cole CV, McClellan JF, Woods LE, Trofymow JA, Elliott ET (1984) Roles of protozoa and nematodes in nutrient cycling. In: Giddens SE, Todd RL (eds) Microbial–plant interactions. ASA, Madison, pp 17–28

    Google Scholar 

  • De Ruiter PC, Van Veen JA, Moore C, Brussaard L, Hunt HW (1993) Calculation of nitrogen mineralization in soil food webs. Plant Soil 157:263–273

    Google Scholar 

  • Diehl S, Feißel M (2000) Effects of enrichment on three-level food chains with omnivory. Am Nat 155:200–218

    Google Scholar 

  • Doncaster CC, Hooper DJ (1961) Nematodes attacked by protozoa and tardigrades. Nematologica 6:333–335

    Google Scholar 

  • Eibye-Jacobsen J (2001) A new method for making SEM preparations of the tardigrade buccopharyngeal apparatus. Zool Anz 240:309–319

    Google Scholar 

  • Elliott ET, Anderson RV, Coleman DC, Cole CV (1980) Habitable pore space and microbial trophic interactions. Oikos 35:327–335

    Google Scholar 

  • Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195–217

    Article  Google Scholar 

  • Gange AC, Brown VK (2002) Soil food web components affect plant community structure during early succession. Ecol Res 17:217–227

    Google Scholar 

  • González-Olivares E, Ramos-Jiliberto R (2003) Dynamic consequences of prey refuges in a simple model system: more prey, fewer predators and enhanced stability. Ecol Model 166:135–146

    Google Scholar 

  • Grootaert P, Jaques A, Small RW (1977) Prey selection in Butlerius sp. (Rhabditida, Diplogasteridae). Meded Fac Landbouwwet Rijksuniv Gent 24:1559–1563

    Google Scholar 

  • Hallas TE, Yeates GW (1972) Tardigrada of the soil and litter of a Danish beach forest. Pedobiologia 12:287–304

    Google Scholar 

  • Hohberg K (2003) Soil nematode fauna of afforested mine sites: genera distribution, trophic structure and functional guilds. Appl Soil Ecol 22:113–126

    Google Scholar 

  • Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91:293–320

    Google Scholar 

  • Huhta V, Sulkava P, Viberg K (1998) Interactions between enchytraeid (Cognettia spagnetorum), microarthropod and nematode populations in forest soil at different moistures. Appl Soil Ecol 9:53–58

    Google Scholar 

  • Hunt HW, Wall DH, DeCrapeo NM, Brenner JS (2001) A model for nematode locomotion in soil. Nematology 3:705–716

    Google Scholar 

  • 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

    Google Scholar 

  • Hyvönen R, Andersson S, Clarholm M, Persson T (1994) Effects of lumbricids and enchytraeids on nematodes in limed and unlimed coniferous mor humus. Biol Fertil Soils 17:201–205

    Google Scholar 

  • Ilieva-Makulec K, Makulec G (2002) Effect of the earthworm Lumbricus rubellus on the nematode community in a peat meadow soil. Eur J Soil Biol 38:59–62

    Google Scholar 

  • Jeschke JM, Tollrian R (2000) Density-dependent effects of prey defences. Oecologia 123:391–396

    Google Scholar 

  • Jeschke JM, Kopp M, Tollrian R (2004) Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol Rev 79:337–349

    Google Scholar 

  • Keeling MJ, Wilson BH, Pacala SW (2000) Reinterpreting space, time lags, and functional responses in ecological models. Science 290:1758–1764

    Google Scholar 

  • Khan Z, Bilgrami AL, Jairajpuri MS (1995) A comparative study on the predation by Allodorylaimus americanus and Discolaimus silvicolus (Nematoda: Dorylaimida) on different species of plant parasitic nematodes. Fundam Appl Nematol 18:99–108

    Google Scholar 

  • Koehler HH (1997) Mesostigmata (Gamasina, Uropodina), efficient predators in agroecosystems. Agric Ecosyst Environ 62:105–117

    Google Scholar 

  • Laakso J, Setälä H (1999) Population- and ecosystem-level effects of predation on microbial-feeding nematodes. Oecologia 120:279–286

    Google Scholar 

  • Manly BFJ, Jamieson CD (1999) Functional response and parallel curve analysis. Oikos 85:523–528

    Google Scholar 

  • Martikainen E, Huhta V (1990) Interactions between nematodes and predatory mites in raw humus soil: a microcosm experiment. Rev Ecol Biol Sol 27:13–20

    Google Scholar 

  • McKee MH, Wrona FJ, Scrimgeour GJ, Culp JM (1997) Importance of consumptive and non-consumptive prey mortality in a coupled predator–prey system. Freshw Biol 38:193–201

    Google Scholar 

  • Mikola J, Setälä H (1998a) No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153–164

    Google Scholar 

  • Mikola J, Setälä H (1998b) Productivity and trophic-level biomasses in a microbial-based soil food web. Oikos 82:158–168

    Google Scholar 

  • Mikola J, Sulkava P (2001) Responses of microbial-feeding nematodes to organic matter distribution and predation in experimental soil habitat. Soil Biol Biochem 33:811–817

    Google Scholar 

  • Moens T, Verbeeck L, Vines M (1999) Feeding biology of a predatory and a facultatively predatory nematode (Enoploides longispiculosus and Adoncholaimus fuscus). Mar Biol 134:585–593

    Google Scholar 

  • Moens T, Herman P, Verbeeck L, Steyaert M, Vincx M (2000) Predation rates and prey selectivity in two predacious estuarine nematode species. Mar Ecol Prog Ser 205:185–193

    Google Scholar 

  • Moore JC, De Ruiter PC (1997) Compartmentalisation of resource utilisation within soil ecosystems. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell Science, Oxford, pp 375–393

    Google Scholar 

  • Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:1–131

    Google Scholar 

  • Murphy IW, Doncaster CC (1957) A culture method for soil meiofauna and its application to the study of nematode predators. Nematologica 2:202–214

    Google Scholar 

  • Nelson DR (2002) Current status of the Tardigrada: evolution and ecology. Integr Comp Biol 42:652–659

    Google Scholar 

  • Nelson DR, Marley NJ (2000) The biology and ecology of lotic Tardigrada. Freshw Biol 44:93–108

    Google Scholar 

  • Nelson DR, McInnes SJ (2002) Tardigrada. In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater meiofauna: biology and ecology. Backhuys Publishers, Leiden, Netherlands, pp 177–215

    Google Scholar 

  • Nicholas WL (1975) The biology of free-living nematodes. Clarendon Press, Oxford

    Google Scholar 

  • Parmelee RW (1995) Soil fauna: linking different levels of the ecological hierarchy. In: Jones CG, Lawton JK (eds) Linking species and ecosystems. Chapman and Hall, New York, pp 107–117

    Google Scholar 

  • Pastorok RA (1981) Prey vulnerability and size selection by Chaoborus larvae. Ecology 62:1311–1324

    Google Scholar 

  • Philips DA, Ferris H, Cook DR, Strong DR (2003) Molecular control points in rhizosphere food webs. Ecology 84:816–826

    Google Scholar 

  • Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383

    Google Scholar 

  • Sayre RM (1969) A method of culturing a predacious tardigrade on the nematode Panagrellus redivivus. Trans Am Microsc Soc 88:266–274

    Google Scholar 

  • Scheu S (2002) The soil food web: structure and perspectives. Eur J Soil Biol 38:11–20

    Google Scholar 

  • Schmid-Araya JM, Schmid PE (2000) Trophic relationships: integrating meiofauna into a realistic benthic food web. Freshw Biol 44:149–163

    Google Scholar 

  • Sih A (1987) Prey refuges and predator–prey stability. Theor Popul Biol 31:1–12

    Google Scholar 

  • Small RW (1987) A review of the prey of predatory soil nematodes. Pedobiologia 30:179–206

    Google Scholar 

  • Small RW, Grootaert P (1983) Observations on the predation abilities of some soil dwelling predatory nematodes. Nematol 29:109–118

    Google Scholar 

  • Sohlenius B (1979) A carbon budget for nematodes, rotifers and tardigrades in a Swedish coniferous forest soil. Holarct Ecol 2:30–40

    CAS  Google Scholar 

  • Sohlenius B (1980) Abundance, biomass and contribution to energy flow by soil nematodes in terrestrial ecosystems. Oikos 34:186–194

    Google Scholar 

  • Traunspurger W (2002) Nematoda. In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater meiofauna: biology and ecology. Backhuys Publishers, Leiden, Netherlands, pp 63–104

    Google Scholar 

  • Traunspurger W, Bergtold M, Goedkopp W (1997) The effects of nematodes on bacterial activity and abundance in a freshwater sediment. Oecologia 112:118–122

    Google Scholar 

  • Wahlström E, Persson L, Diehl S, Byström P (2000) Size-dependent foraging efficiency, cannibalism and zooplankton community structure. Oecologia 123:138–148

    Google Scholar 

  • Wallace HR (1958) Movement of eelworms. Ann Appl Biol 46:662–668

    Google Scholar 

  • Walter DE, Hudgens RA, Freckman DW (1986) Consumption of nematodes by fungivorous mites, Tyrophagus spp (Acarina: Astigmata: Acaridae). Oecologia 70:357–361

    Google Scholar 

  • Wardle DA (1995) Impacts of disturbance on detritus food webs in agro-ecosystems of contrasting tillage and weed management practices. Adv Ecol Res 26:105–185

    Google Scholar 

  • Wasilewska L (2000) The effect of macroarthropods patrolling soil surface on soil nematodes: a field experiment in a mown meadow. Pol J Ecol 48:327–338

    Google Scholar 

  • Yeates GW (1969) Predation by Mononchoides potohikus (Nematoda: Diplogateridae) in laboratory culture. Nematologica 15:1–9

    Google Scholar 

  • Yeates GW (1987) Nematode feeding and activity: the importance of development stages. Biol Fertil Soils 3:143–146

    Google Scholar 

  • Yeates GW, Foissner W (1995) Testate amoebae as predators of nematodes. Biol Fertil Soils 20:1–7

    Google Scholar 

  • Yeates GW, Wardle DA (1996) Nematodes as predators and prey: relationships to biological control and soil processes. Pedobiologia 40:43–50

    Google Scholar 

  • Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331

    Google Scholar 

  • Yeates GW, Dando JL, Shepherd TG (2002) Pressure plate studies to determine how moisture affects access of bacterial-feeding nematodes to food in soil. Eur J Soil Sci 53:355–365

    Google Scholar 

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Acknowledgements

We thank Hartmut Greven and Jonathan M. Jeschke who commented on earlier versions of this paper. The experiments comply with the current laws of Germany.

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Correspondence to Karin Hohberg.

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Hohberg, K., Traunspurger, W. Predator–prey interaction in soil food web: functional response, size-dependent foraging efficiency, and the influence of soil texture. Biol Fertil Soils 41, 419–427 (2005). https://doi.org/10.1007/s00374-005-0852-9

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  • DOI: https://doi.org/10.1007/s00374-005-0852-9

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