, Volume 707, Issue 1, pp 159–172 | Cite as

Bottom-up effects on freshwater bacterivorous nematode populations: a microcosm approach

  • A. Gaudes
  • I. Muñoz
  • T. Moens
Primary Research Paper


Nutrient enrichment may alter population dynamics of species in different ways depending on their life strategies. The aim of this study was to test the effect of different nutrient concentrations on the population development of two bacterivorous freshwater nematodes, Bursilla monhystera and Plectus aquatilis. Microcosms with autoclaved natural sand from a pristine stream (Fuirosos, NE of Spain) were enriched with different levels of phosphate, nitrate and ammonia as inorganic nutrients and glucose as a biodegradable dissolved organic carbon source. Although leaching of carbon and nutrients from the detritus fraction in the sediment initially may have overruled differences between treatments, later samplings revealed bottom-up control, with Bursilla monhystera abundances positively correlated to bacterial abundances at high nutrient concentrations. Nevertheless, there were several indications that nematodes in turn affected microbial abundance, most likely through excretion of ammonia and through grazing. In contrast to B. monhystera, Plectus aquatilis at high nutrient concentrations showed a unimodal abundance curve, while not increasing in abundance at low nutrient concentrations. Glucose enrichment did not have any stimulatory effect on either microbial or nematode abundances, probably as a result of unfavourable C:N:P stoichiometry. P enrichment, by contrast, stimulated microbial and Bursilla abundances. Our results indicate that episodic nutrient enrichment may affect populations of bacterial-feeding nematodes in the short term. Their longer-term dynamics may, however, be more dependent on leaching of carbon and nutrients from the pools of sediment-bound detritus.


Eutrophication Nematodes Bacteria Bottom-up Top-down control 



Financial support for the experiments reported here was obtained from Ghent University through BOF project 0110600002 from the Flemish Science Foundation FWO through project G.0192.09 and from University of Barcelona trough SCARCE-Consolider project from the Spanish Ministry. Claudia Höckelmann kindly provided the Lake Zürich samples from which the Plectus aquatilis culture was isolated. Esther Mas, Giovani P. dos Santos, Dirk Van Gansbeke and Tania Nara Bezerra also contributed to sample processing. We also thank the editor and two anonymous reviewers for their helpful comments on the manuscript.

Supplementary material

10750_2012_1421_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 kb)


  1. Abebe, E., W. Decraemer & P. De Ley, 2008. Global diversity of nematodes (Nematoda) in freshwater. Developments in Hydrobiology 198: 67–78.CrossRefGoogle Scholar
  2. Abrams, B. I. & M. J. Mitchell, 1980. Role of nematode-bacterial interactions in heterotrophic systems with emphasis on sewage sludge decomposition. Oikos 35: 404–410.CrossRefGoogle Scholar
  3. Alkemade, R., A. Wielemaker & M. A. Hemminga, 1992a. Stimulation of Spartina anglica leaves by the bacterivorous marine nematode Diplolaimelloides bruciei. Journal of Experimental Marine Biology and Ecology 159: 267–278.CrossRefGoogle Scholar
  4. Alkemade, R., A. Wielemaker, S. A. de Jong & A. J. J. Sandee, 1992b. Experimental evidence for the role of bioturbation by the marine nematode Diplolaimella dievengatensis in stimulating the mineralization of Spartina anglica detritus. Marine Ecology Progress Series 90: 149–155.CrossRefGoogle Scholar
  5. Anderson, R. V. & D. C. Coleman, 1981. Population development and interactions between two species of bacteriophagic nematodes. Nematologica 27: 6–19.CrossRefGoogle Scholar
  6. Artigas, J., A. M. Romaní, A. Gaudes, I. Muñoz & S. Sabater, 2009. Organic matter availability structures microbial biomass and activity in a Mediterranean stream. Freshwater Biology 54: 2025–2036.CrossRefGoogle Scholar
  7. Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289–300.Google Scholar
  8. Bongers, T., 1999. The Maturity Index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant and Soil 212: 13–22.CrossRefGoogle Scholar
  9. Bonkowski, M., B. Griffiths & C. Scrimgeour, 2000. Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Applied Soil Ecology 14: 37–53.CrossRefGoogle Scholar
  10. Bouwman, L. A., J. Bloem, P. H. J. F. van den Boogert, F. Bremer, G. H. J. Hoenderboem & P. C. de Ruiter, 1994. Short-term and long-term effects of bacterivorous nematodes and nematophagous fungi on carbon and nitrogen mineralization in microcosms. Biology and Fertility of Soils 17: 249–256.CrossRefGoogle Scholar
  11. Coleman, D. C., C. V. Cole, R. V. Anderson, M. Blaha, M. K. Campion, M. Clarholm, E. T. Elliott, H. W. Hunt, B. Shaefer & J. Sinclair, 1977. An analysis of rhizosphere-saprophage interactions in terrestrial ecosystems. In Lohm U. L. & T. Persson (eds), Soil Organisms as Components of Ecosystems. Ecological Bulletin Number 25, Swedish National Research Council. Stockholm: 299–309.Google Scholar
  12. Cross, W. F., B. R. Johnson, J. B. Wallace & A. D. Rosemond, 2005. Contrasting response of stream detritivores to long-term nutrient enrichment. Limnology and Oceanography 50: 1730–1739.CrossRefGoogle Scholar
  13. Cross, W. F., J. B. Wallace & A. D. Rosemond, 2007. Nutrient enrichment reduces constraints on material flows in a detritus-based food web. Ecology 88: 2563–2575.PubMedCrossRefGoogle Scholar
  14. De Mesel, I., S. Derycke, J. Swings, M. Vincx & T. Moens, 2003. Influence of bacterivorous nematodes on the decomposition of cordgrass. Journal of Experimental Marine Biology and Ecology 296: 227–242.CrossRefGoogle Scholar
  15. De Mesel, I., S. Derycke, T. Moens, K. van der Gucht, M. Vincx & J. Swings, 2004. Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environmental Microbiology 6: 733–744.PubMedCrossRefGoogle Scholar
  16. De Mesel, I., S. Derycke, J. Swings, M. Vincx & T. Moens, 2006. Role of nematodes in decomposition processes: does within-trophic group diversity matter? Marine Ecology Progress Series 321: 157–166.CrossRefGoogle Scholar
  17. Derycke, S., R. van Vynckt, J. Vanoverbeke, M. Vincx & T. Moens, 2007. Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and genetic structure of the dominant species Pellioditis marina. Limnology and Oceanography 52: 992–1001.CrossRefGoogle Scholar
  18. Elser, J. J., & D. O. Hessen, 2005. Biosimplicity via stochiometry: the evolution of food-web structure and processes. In Belgrano, A., U. Scharler, J. Dunne & R. Ulanowicz (eds), Aquatic Food Webs: An Ecosystem Approach. Oxford University Press, UK.Google Scholar
  19. Elser, J. J., K. Hayakawa & J. Urabe, 2001. Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82: 898–903.Google Scholar
  20. Feller, R. J. & R. M. Warwick, 1988. Energetics. In Higgins, R. P. & H. Thiel (eds), Introduction to the Study of Meiofauna. Smithsonian Institution. London, UK.Google Scholar
  21. Ferris, H., S. S. Lau & R. C. Venette, 1995. Population energetics of bacterial-feeding nematodes: respiration and metabolic rates based on carbon dioxide production. Soil Biology and Biochemistry 27: 319–330.CrossRefGoogle Scholar
  22. Ferris, H., M. Eyre, R. C. Venette & S. S. Lau, 1996. Population energetics of bacterial-feeding nematodes: stage-specific development and fecundity rates. Soil Biology and Biochemistry 28: 271–280.CrossRefGoogle Scholar
  23. Ferris, H., R. C. Venette & S. S. Lau, 1997. Population energetics of bacterial-feeding nematodes: carbon and nitrogen budgets. Soil Biology and Biochemistry 29: 1183–1194.CrossRefGoogle Scholar
  24. Ferris, H., R. C. Venette, H. R. van der Meulen & S. S. Lau, 1998. Nitrogen mineralization by bacterial-feeding nematodes: verification and measurement. Plant and Soil 203: 159–171.CrossRefGoogle Scholar
  25. Findlay, S. & K. R. Tenore, 1982. Effect of a free-living marine nematode (Diplolaimella chitwoodi) on detrital carbon mineralization. Marine Ecology Progress Series 8: 161–166.CrossRefGoogle Scholar
  26. Freckman, D. W., 1988. Bacterivorous nematodes and organic-matter decomposition. Agriculture, Ecosystems and Environment 24: 195–217.CrossRefGoogle Scholar
  27. Gaudes, A., S. Sabater, E. Vilalta & I. Muñoz, 2006. The nematode community in cyanobacterial biofilms in the river Llobregat. Spain. Nematology. 8: 909–919.CrossRefGoogle Scholar
  28. Gaudes, A., J. Ocaña & I. Muñoz, 2012. Meiofaunal response to nutrient addition in a Mediterranean stream. Freshwater Biology. doi: 10.1111/j.1365-2427.2012.02757.x
  29. Greenwood, J. L., A. D. Rosemond, J. B. Wallace, W. F. Cross & H. S. Weyers, 2007. Nutrients stimulate leaf breakdown rates and detritivore biomass: bottom-up effects via heterotrophic pathways. Oecologia 151: 637–649.PubMedCrossRefGoogle Scholar
  30. Griffiths, B. S., 1994. Microbial-feeding nematodes and Protozoa in soil: their effects on microbial activity and nitrogen mineralization in decomposition hotspots and the rhizosphere. Plant and Soil 164: 25–33.CrossRefGoogle Scholar
  31. Gulis, V. & K. Suberkropp, 2003. Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshwater Biology 48: 123–134.CrossRefGoogle Scholar
  32. Gulis, V., A. D. Rosemond, K. Suberkropp, H. S. Weyers & J. P. Benstead, 2004. Effects of nutrient enrichment on the decomposition of wood and associated microbial activity in streams. Freshwater Biology. 49: 1437–1447.CrossRefGoogle Scholar
  33. Heip, C., M. Vincx & G. Vranken, 1985. The ecology of marine nematodes. Oceanography and Marine Biology Annual Review 23: 399–489.Google Scholar
  34. Hillebrand, H., M. Kahlert, A. L. Haglund, U. G. Berninger, S. Nagel & S. Wickham, 2002. Control of microbenthic communities by grazing and nutrient supply. Ecology 83: 2205–2219.CrossRefGoogle Scholar
  35. Hodda, M., 2006. Nematodes in lotic systems. In Abebe, E., W. Traunspurger & I. Andrássy (eds), Freshwater Nematodes: Ecology and Taxonomy. CABI Publishing. Oxfordshire, UK.Google Scholar
  36. Hodda, M., A. Ocaña & W. Traunspurger, 2006. Nematodes from extreme freshwater habitats. In Abebe, E., W. Traunspurger & I. Andrássy (eds), Freshwater Nematodes: Ecology and Taxonomy. CABI Publishing. Oxfordshire, UK.Google Scholar
  37. Höss, S., M. Bergtold, M. Haitzer, W. Traunspurger & C. E. W. Steinberg, 2001. Refractory dissolved organic matter can influence the reproduction of Caenorhabditis elegans (Nematoda). Freshwater Biology 46: 1–10.CrossRefGoogle Scholar
  38. Ingham, E. R., J. A. Trofymore, E. R. Ingham & D. C. Coleman, 1985. Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecological Monographs 55: 119–140.CrossRefGoogle Scholar
  39. Johannes, R. E., 1965. Influence of marine protozoa on nutrient regeneration. Limnology and Oceanography 10: 434–442.CrossRefGoogle Scholar
  40. Kammenga, J. E., C. A. M. Van Gestel & J. Bakker, 1994. Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Archives of Environmental Contamination and Toxicology 27: 88–94.PubMedCrossRefGoogle Scholar
  41. Lee, D. L. & H. J. Atkinson, 1977. Physiology of Nematodes. Columbia University Press, New York.Google Scholar
  42. Lopez-Doval, J. C., M. Großschartner, S. Höss, C. Orendt, W. Traunspurger, G. Wolfram & I. Muñoz, 2010. Invertebrate communities in soft sediments along a pollution gradient in a Mediterranean river (Llobregat, NE Spain). Limnetica 29: 311–322.Google Scholar
  43. Marchant, R. & W. L. Nicholas, 1974. An energy budget for the free-living nematode Pelodera (Rhabditidae). Oecologia 16: 237–252.CrossRefGoogle Scholar
  44. Martínez, J. G., G. A. P. dos Santos, S. Derycke & T. Moens, 2012. Effects of cadmium on the fitness of, and interactions between, two bacterivorous nematode species. Applied Soil Ecology 56: 10–18.Google Scholar
  45. Moens, T. & M. Vincx, 1998. On the cultivation of free-living estuarine and marine nematodes. Helgol. Meeresunters 52: 115–139.CrossRefGoogle Scholar
  46. Moens, T., G. A. P. dos Santos, F. Thompson, J. Swings, V. Fonsêca-Genevois, M. Vincx & I. De Mesel, 2005. Do nematode mucus secretions affect bacterial growth? Aquatic Microbial Ecology 40: 77–83.CrossRefGoogle Scholar
  47. Postma-Blaauw, M. B., F. T. de Vries, R. G. de Goede, M. J. Bloem, J. H. Faber & L. Brussaard, 2005. Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142: 428–439.PubMedCrossRefGoogle Scholar
  48. Riemann, F. & E. Helmke, 2002. Symbiotic relations of sediment-agglutinating nematodes and bacterial in detrital habitats: The Enzyme-Sharing Concept. Marine Ecology 23: 93–113.CrossRefGoogle Scholar
  49. Ristau, K. & W. Traunspurger, 2011. Relation between nematode communities and trophic state in southern Swedish lakes. Hydrobiologia 663: 121–133.CrossRefGoogle Scholar
  50. Sabater, S. & K. Tockner, 2010. Effects of hydrologic alterations in the ecological quality of river ecosystems. In Sabater, S. & D. Barceló (eds), Water Scarcity in Mediterranean Areas. Springer, BerlinGoogle Scholar
  51. Sabater, S., J. Artigas, A. Gaudes, I. Muñoz, G. Urrea & A. M. Romaní, 2011. Longterm moderate nutrient inputs enhance autotrophy in a forested Mediterranean stream. Freshwater Biology. doi: 10.1111/j.1365-2427.2010.02567.x.Google Scholar
  52. Schiemer, F., 1982. Food dependence and energetics of freeliving nematodes. I. Respiration, growth and reproduction of Caenorhabditis briggsae (Nematoda) at different levels of food supply. Oecologia 54: 108–121.CrossRefGoogle Scholar
  53. Schiemer, F., 1983. Food dependence and energetics of free-living nematodes. III. Comparative aspects with special consideration of two bacterivorous species Caenorhabditis briggsae and Plectus palustris. Oikos 41: 32–43.CrossRefGoogle Scholar
  54. Schiemer, F., 1985. Bioenergetic niche differentiation of aquatic invertebrates. Verhandlungen der Internazionale Vereinigung für Theoretische und Angewandte Limnologie 22: 3014–3018.Google Scholar
  55. Schroeder, F., W. Traunspurger, K. Pettersson & L. Peters, 2012. Temporal changes in periphytic meiofauna in lakes of different trophic states. Journal of Limnology 71: 216–227.CrossRefGoogle Scholar
  56. Sudhaus, W., 1980. Systematisch-phylogenetische und biologisch-ökologische Untersuchungen an Rhabditis- (Poikilolaimus-) Arten als Beitrag zur Rassenbildung und Parallelevolution bei Nematoden. Zool. Jb. syst. 107: 287–343.Google Scholar
  57. Traunspurger, W., 2002. Nematoda. In Rundle, S. D., A. L. Robertson & J. M. Schmid-Araya (eds), Freshwater Meiofauna: Biology and Ecology. Backhuys Publishers. The Netherlands, Leiden.Google Scholar
  58. Traunspurger, W., M. Bergtold & W. Goodkoep, 1997. The effect of nematodes on activity and abundance of bacteria in a profundal freshwater sediment. Oecologia 112: 118–122.CrossRefGoogle Scholar
  59. Venette, R. C. & H. Ferris, 1997. Thermal constraints to population growth of bacterial-feeding nematodes. Soil Biology and Biochemistry 29: 63–74.CrossRefGoogle Scholar
  60. Warwick, R. M. & R. Price, 1979. Ecological and metabolic studies on free-living nematodes from an estuarine mud-flat. Estuarine and Coastal Marine Science 9: 257–271.CrossRefGoogle Scholar
  61. Waters, T. F., 1977. Secondary production in inland waters. Advances in Ecological Research 10: 91–164.CrossRefGoogle Scholar
  62. Wieser, W., 1960. Benthic studies in Buzzards Bay II. The Meiofauna. Limnology and Oceanography 5: 121–137.CrossRefGoogle Scholar
  63. Woombs, M & J. Laybourn-Parry, 1985. Energy partitioning in three species of nematodes from polysaprobic environments. Oecologia 65: 289–295.Google Scholar
  64. Yeates, G. W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils 37: 199–210.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Departament d’Ecologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Marine Biology Lab, Biology DepartmentGhent UniversityGhentBelgium

Personalised recommendations