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Feeding of biofilm-dwelling nematodes examined using HPLC-analysis of gut pigment contents

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Abstract

The natural feeding behaviour of the nematodes Chromadorina bioculata (Schultze in Carus 1857) and Chromadorina viridis (Linstow 1876) was studied in situ, within epilithic biofilms of the Garonne River (France). Based on their feeding-type characteristics and population dynamics, it was hypothesised that these species feed selectively on microphytobenthos (MPB) within the biofilm, and that among MPB groups, diatoms are preferred. High-performance liquid chromatography (HPLC) was used for separation, identification and quantification of pigments both in nematode guts and in the biofilm. This is the first time that nematode gut pigment contents were examined under natural conditions. Diatoms dominated the MPB which also comprised cyanobacteria and green microalgae. The comparison between chlorophyll a content in nematode guts versus in the biofilm showed that C. bioculata and C. viridis fed opportunistically (non-selectively) on MPB within the biofilm. Only diatom biomarker pigments were found in nematode guts suggesting that they could preferentially fed on diatoms among MPB groups. However, the non-detection of biomarker pigments for other microphyte groups could be also linked to HPLC detection limits. It was estimated that Chromadorina nematodes daily ingested on average 0.03–0.67% of the MPB standing stock. This grazing covered only a small part of their energetic requirements, suggesting that besides MPB they probably also fed on other biofilm food sources. Some considerations on the applicability of the HPLC gut pigment analysis technique for the examination of nematode feeding are also presented.

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References

  • Ameziane, T., A. Dauta & R. Le Cohu, 2003. Origin and transport of phytoplankton in a large river: the Garonne, France. Archiv für Hydrobiologie 156: 385–404.

    Article  Google Scholar 

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

    Google Scholar 

  • Avery, L. & J. H. Thomas, 1997. Feeding and defecation. In Riddle, D. L., T. Blumenthal, B. J. Meyer & J. R. Priess (eds), C. elegans II, 2nd ed. Cold Spring Harbor Laboratory Press, New York: 679–716.

    Google Scholar 

  • Barlow, R. G., D. G. Cummings & S. W. Gibb, 1997. Improved resolution of mono-and divinyl chlorophylls a and b and zeaxanthin and lutein in phytoplankton extracts using reverse phase C-8 HPLC. Marine Ecology Progress Series 161: 303–307.

    Article  CAS  Google Scholar 

  • Bergtold, M. & W. Traunspurger, 2005. Benthic production by micro-, meio-, and macrobenthos in the profundal zone of an oligotrophic lake. Journal of the North American Benthological Society 24: 321–329.

    Article  Google Scholar 

  • Bilgrami, A. L. & R. Gaugler, 2005. Feeding behaviour of the predatory nematodes Laimydorus baldus and Discolaimus major (Nematoda: Dorylaimida). Nematology 7: 11–20.

    Article  Google Scholar 

  • Bilgrami, A. L., I. Ahmad & S. Jairajpuri, 1984. Predatory behaviour of Aquatides thornei (Nygolaimina: Nematoda). Nematologica 30: 457–462.

    Article  Google Scholar 

  • Borchardt, M. A. & T. L. Bott, 1995. Grazing of bacteria and algae in a Piedmont stream. Journal of the North American Benthological Society 14: 278–298.

    Article  Google Scholar 

  • Boulêtreau, S., F. Garabetian, S. Sauvage & J. M. Sanchez-Perez, 2006. Assessing the importance of a self-generated detachment process in river biofilm models. Freshwater Biology 51: 901–912.

    Article  Google Scholar 

  • Brotas, V. & M. R. Plante-Cuny, 1998. Spatial and temporal patterns of microphytobenthic taxa of estuarine tidal flats in the Tagus Estuary (Portugal) using pigment analysis by HPLC. Marine Ecology Progress Series 171: 43–57.

    Article  Google Scholar 

  • Buffan-Dubau, E. & K. R. Carman, 2000. Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnology and Oceanography 45: 381–395.

    Article  CAS  Google Scholar 

  • Buffan-Dubau, E., R. de Wit & J. Castel, 1996. Feeding selectivity of the harpacticoid copepod Canuella perplexa in benthic muddy environments demonstrated by HPLC analyses of chlorin and carotenoid pigments. Marine Ecology Progress Series 137: 71–82.

    Article  CAS  Google Scholar 

  • Butkas, K., Y. Vadeboncoeur & M. Vander Zanden, 2011. Estimating benthic invertebrate production in lakes: a comparison of methods and scaling from individual taxa to the whole-lake level. Aquatic Sciences 73: 153–169.

    Article  CAS  Google Scholar 

  • Chauvet, E. & H. Décamps, 1989. Lateral interactions in a fluvial landscape: the river Garonne, France. Journal of the North American Benthological Society 8: 9–17.

    Article  Google Scholar 

  • Croll, N. A. & A. Zullini, 1972. Observations on the bionomics of the freshwater nematode Chromadorina bioculata. Journal of Nematology 4: 256–260.

    PubMed  CAS  Google Scholar 

  • Decraemer, W. & N. Smol, 2006. Orders Chromadorida, desmodorida and desmoscolecida. In Abebe, E., W. Traunspurger & I. Andrassy (eds), Freshwater Nematodes: Ecology and Taxonomy. CABI publishing, Wallingford: 163–178.

    Google Scholar 

  • Deutsch, A., 1978. Gut ultrastructure and digestive physiology of two marine nematodes, Chromadorina germanica (Bütschli, 1874) and Diplolaimella sp. Biological Bulletin 155: 317–335.

    Article  Google Scholar 

  • Duncan, A., F. Schiemer & R. Z. Klekowski, 1974. A preliminary study of feeding rates on bacterial food by adult females of a benthic nematode, Plectus palustris De Man 1880. Polish Archives of Hydrobiology 21: 249–255.

    Google Scholar 

  • Epstein, S. S. & M. P. Shiaris, 1992. Rates of microbenthic and meiobenthic bacterivory in a temperate muddy tidal flat community. Applied and Environmental Microbiology 58: 2426–2431.

    PubMed  CAS  Google Scholar 

  • Evrard, V., K. Soetaert, C. H. R. Heip, M. Huettel, M. A. Xenopoulos & J. J. Middelburg, 2010. Carbon and nitrogen flows through the benthic food web of a photic subtidal sandy sediment. Marine Ecology Progress Series 416: 1–16.

    Article  CAS  Google Scholar 

  • Flemming, H. C. & J. Wingender, 2010. The biofilm matrix. Nature Reviews Microbiology 8: 623–633.

    PubMed  CAS  Google Scholar 

  • Gasparini, S., J. Castel & X. Irigoien, 1999. Impact of suspended particulate matter on egg production of the estuarine copepod, Eurytemora affinis. Journal of Marine Systems 22: 195–205.

    Article  Google Scholar 

  • Gaudes, A., S. Sabater, E. Vilalta & I. Muñoz, 2006. The nematode community in cyanobacterial biofilms in the river Llobregat, Spain. Nematology 8: 909–919.

    Article  Google Scholar 

  • Ghafouri, S. & J. D. McGhee, 2007. Bacterial residence time in the intestine of Caenorhabditis elegans. Nematology 9: 87–91.

    Article  Google Scholar 

  • Goedkoop, W. & R. K. Johnson, 1996. Pelagic-benthic coupling: profundal benthic community response to spring diatom deposition in mesotrophic Lake Erken. Limnology and Oceanography 41: 636–647.

    Article  CAS  Google Scholar 

  • Goldfinch, A. C. & K. R. Carman, 2000. Chironomid grazing on benthic microalgae in a Louisiana salt marsh. Estuaries 23: 536–547.

    Article  Google Scholar 

  • Hamels, I., T. Moens, K. Muylaert & W. Vyverman, 2001. Trophic interactions between ciliates and nematodes from an intertidal flat. Aquatic Microbial Ecology 26: 61–72.

    Article  Google Scholar 

  • Heip, C., R. Huys, M. Vincx, A. Vanreusel, N. Smol, R. Herman & P. M. J. Herman, 1990. Composition, distribution, biomass and production of North Sea meiofauna. Netherlands Journal of Sea Research 26: 333–342.

    Article  Google Scholar 

  • Herman, P. M. J. & G. Vranken, 1988. Studies of the life-history and energetics of marine and brackish-water nematodes. II. Production, respiration and food uptake by Monhystera disjuncta. Oecologia 77: 457–463.

    Article  Google Scholar 

  • Höckelmann, C., T. Moens & F. Jüttner, 2004. Odor compounds from cyanobacterial biofilms acting as attractants and repellents for free-living nematodes. Limnology and Oceanography 49: 1809–1819.

    Article  Google Scholar 

  • Hodda, M. & E. Abebe, 2006. Techniques for processing freshwater nematodes. In Abebe, E., W. Traunspurger & I. Andrassy (eds), Freshwater Nematodes: Ecology and Taxonomy. CABI Publishing, Wallingford, UK: 31–45.

    Chapter  Google Scholar 

  • Holling, C. S., 1959. Some characteristics of simple types of predation and parasitism. Canadian entomologist 91: 385–398.

    Article  Google Scholar 

  • Irigoien, X., R. N. Head, R. P. Harris, D. Cummings, D. Harbour & B. Meyer-Harms, 2000. Feeding selectivity and egg production of Calanus helgolandicus in the English Channel. Limnology and Oceanography 45: 44–54.

    Article  Google Scholar 

  • Jeffrey, S. W., R. F. C. Mantoura & S. W. Wright, 1997. Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods. UNESCO publishing, Paris, France: 661.

    Google Scholar 

  • Jensen, P., 1982. Diatom-feeding behaviour of the free-living marine nematode Chromadorita tenuis. Nematologica 28: 71–76.

    Article  Google Scholar 

  • Johansen, J. E., W. A. Svec, S. Liaaen-Jensen & F. T. Haxo, 1974. Carotenoids of the dinophyceae. Phytochemistry 13: 2261–2271.

    Article  CAS  Google Scholar 

  • Lamberti, G. A. & V. H. Resh, 1983. Stream periphyton and insect herbivores: an experimental study of grazing by a caddisfly population. Ecology 64: 1124–1135.

    Article  Google Scholar 

  • Leflaive, J., S. Boulêtreau, E. Buffan-Dubau & L. Ten-Hage, 2008. Temporal patterns in epilithic biofilm-relation with a putative allelopathic activity. Fundamental and Applied Limnology 173: 121–134.

    Article  CAS  Google Scholar 

  • Lyautey, E., C. R. Jackson, J. Cayrou, J. L. Rols & F. Garabetian, 2005. Bacterial community succession in natural river biofilm assemblages. Microbial Ecology 50: 589–601.

    Article  PubMed  Google Scholar 

  • Mackey, M. D., D. J. Mackey, H. W. Higgins & S. W. Wright, 1996. CHEMTAX—a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Marine Ecology Progress Series 144: 265–283.

    Article  CAS  Google Scholar 

  • Majdi, N., W. Traunspurger, S. Boyer, B. Mialet, M. Tackx, R. Fernandez, S. Gehner, L. Ten-Hage & E. Buffan-Dubau, 2011. Response of biofilm-dwelling nematodes to habitat changes in the Garonne River, France: influence of hydrodynamics and microalgal availability. Hydrobiologia 673: 229–244.

    Article  CAS  Google Scholar 

  • Majdi, N., B. Mialet, S. Boyer, M. Tackx, J. Leflaive, S. Boulêtreau, L. Ten-Hage, F. Julien, R. Fernandez & E. Buffan-Dubau, 2012. The relationship between epilithic biofilm stability and its associated meiofauna under two patterns of flood disturbance. Journal of the North American Benthological Society. 31(1).

  • Mathieu, M., J. Leflaive, L. Ten-Hage, R. de Wit & E. Buffan-Dubau, 2007. Free-living nematodes affect oxygen turnover of artificial diatom biofilms. Aquatic Microbial Ecology 49: 281–291.

    Article  Google Scholar 

  • Meschkat, A., 1934. Der Bewuchs in der Röhrichten des Plattensees. Archiv für Hydrobiologie 27: 436–517.

    Google Scholar 

  • Moens, T. & M. Vincx, 1997. Observations on the feeding ecology of estuarine nematodes. Journal of the Marine Biological Association of the UK 77: 211–227.

    Article  Google Scholar 

  • Moens, T. & M. Vincx, 2000. Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments. Journal of Experimental Marine Biology and Ecology 243: 137–154.

    Article  Google Scholar 

  • Moens, T., L. Verbeeck & M. Vincx, 1999. Preservation and incubation time-induced bias in tracer-aided grazing studies on meiofauna. Marine Biology 133: 69–77.

    Article  Google Scholar 

  • Moens, T., C. Luyten, J. J. Middelburg, P. M. J. Herman & M. Vincx, 2002. Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Marine Ecology Progress Series 234: 127–137.

    Article  Google Scholar 

  • Moens, T., W. Traunspurger & M. Bergtold, 2006. Feeding ecology of free-living benthic nematodes. In Abebe, E., W. Traunspurger & I. Andrassy (eds), Freshwater Nematodes: Ecology and Taxonomy. CABI Publishing, Wallingford: 105–131.

    Chapter  Google Scholar 

  • Montagna, P. A., G. F. Blanchard & A. Dinet, 1995. Effect of production and biomass of intertidal microphytobenthos on meiofaunal grazing rates. Journal of Experimental Marine Biology and Ecology 185: 149–165.

    Article  Google Scholar 

  • Murga, R., P. S. Stewart & D. Daly, 1995. Quantitative analysis of biofilm thickness variability. Biotechnology and Bioengineering 45: 503–510.

    Article  PubMed  CAS  Google Scholar 

  • Nicholas, W. L., A. Grassia & S. Viswanathan, 1973. The efficiency with which Caenorhabditis briggsae (Rhabditidae) feeds on the bacterium, Escherichia coli. Nematologica 19: 411–420.

    Article  Google Scholar 

  • Nielsen, P. H., A. Jahn & R. Palmgren, 1997. Conceptual model for production and composition of exopolymers in biofilms. Water Science and Technology 36: 11–19.

    Article  CAS  Google Scholar 

  • Nozais, C., M. Gosselin, C. Michel & G. Tita, 2001. Abundance, biomass, composition and grazing impact of the sea-ice meiofauna in the north water, northern Baffin Bay. Marine Ecology Progress Series 217: 235–250.

    Article  Google Scholar 

  • Pascal, P. Y., C. Dupuy, P. Richard, J. Rzeznik-Orignac & N. Niquil, 2008. Bacterivory of a mudflat nematode community under different environmental conditions. Marine Biology 154: 671–682.

    Article  Google Scholar 

  • Peters, R. H., 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge: 333.

    Google Scholar 

  • Peters, L. & W. Traunspurger, 2005. Species distribution of free-living nematodes and other meiofauna in littoral periphyton communities of lakes. Nematology 7: 267–280.

    Article  Google Scholar 

  • Phillips, N. W., 1984. Role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bulletin of Marine Science 35: 283–298.

    Google Scholar 

  • Pinckney, J. L., K. R. Carman, S. E. Lumsden & S. N. Hymel, 2003. Microalgal-meiofaunal trophic relationships in muddy intertidal estuarine sediments. Aquatic Microbial Ecology 31: 99–108.

    Article  Google Scholar 

  • Plante, C. & J. A. Downing, 1989. Production of freshwater invertebrate populations in lakes. Canadian Journal of Fisheries and Aquatic Sciences 46: 1489–1498.

    Article  Google Scholar 

  • Price, H. J., 1988. Feeding mechanisms in marine and freshwater zooplankton. Bulletin of Marine Science 43: 327–343.

    Google Scholar 

  • Reiss, J. & J. M. Schmid-Araya, 2010. Life history allometries and production of small fauna. Ecology 91: 497–507.

    Article  PubMed  Google Scholar 

  • Reiss, J., J. Forster, F. Cassio, C. Pascoal, R. Stewart & A. G. Hirst, 2010. When microscopic organisms inform general ecological theory. In Woodward, G. (ed.), Integrative Ecology: From Molecules to Ecosystems. Academic Press, Oxford, UK: 45–77.

    Chapter  Google Scholar 

  • Riemann, F. & E. Helmke, 2002. Symbiotic relations of sediment-agglutinating nematodes and bacteria in detrital habitats: the enzyme-sharing concept. Marine Ecology 23: 93–113.

    Article  CAS  Google Scholar 

  • Riemann, F. & M. Schrage, 1978. The mucus-trap hypothesis on feeding of aquatic Nematodes and implications for biodegradation and sediment texture. Oecologia 34: 75–88.

    Article  Google Scholar 

  • Romeyn, K. & L. A. Bouwman, 1983. Food selection and consumption by estuarine nematodes. Aquatic Ecology 17: 103–109.

    Google Scholar 

  • Ruess, L., M. M. Häggblom, E. J. García Zapata & J. Dighton, 2002. Fatty acids of fungi and nematodes-possible biomarkers in the soil food chain? Soil Biology and Biochemistry 34: 745–756.

    Article  CAS  Google Scholar 

  • Rzeznik-Orignac, J., D. Fichet & G. Boucher, 2003. Spatio-temporal structure of the nematode assemblages of the Brouage mudflat (Marennes Oleron, France). Estuarine Coastal and Shelf Science 58: 77–88.

    Article  CAS  Google Scholar 

  • Sabater, S., E. Vilalta, A. Gaudes, H. Guasch, I. Munoz & A. Romani, 2003. Ecological implications of mass growth of benthic cyanobacteria in rivers. Aquatic Microbial Ecology 32: 175–184.

    Article  Google Scholar 

  • Schagerl, M., C. Pichler & K. Donabaum, 2003. Patterns of major photosynthetic pigments in freshwater algae. 2. Dinophyta, Euglenophyta, Chlorophyceae and Charales. International Journal of Limnology 39: 49–62.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Schmid-Araya, J. M. & P. E. Schmid, 2000. Trophic relationships: integrating meiofauna into a realistic benthic food web. Freshwater Biology 44: 149–163.

    Article  Google Scholar 

  • Schmid-Araya, J. M., A. G. Hildrew, A. Robertson, P. E. Schmid & J. Winterbottom, 2002. The importance of meiofauna in food webs: evidence from an acid stream. Ecology 83: 1271–1285.

    Article  Google Scholar 

  • Stauber, J. L. & S. W. Jeffrey, 1988. Photosynthetic pigments in fifty-one species of marine diatoms. Journal of Phycology 24: 158–172.

    CAS  Google Scholar 

  • Stead, T. K., J. M. Schmid-Araya & A. G. Hildrew, 2005. Secondary production of a stream metazoan community: does the meiofauna make a difference? Limnology and Oceanography 50: 398–403.

    Article  Google Scholar 

  • Tackx, M. L. M., P. J. M. Herman, S. Gasparini, X. Irigoien, R. Billiones & M. H. Daro, 2003. Selective feeding of Eurytemora affinis (Copepoda, Calanoida) in temperate estuaries: model and field observations. Estuarine Coastal and Shelf Science 56: 305–311.

    Article  Google Scholar 

  • Tietjen, J. H. & J. J. Lee, 1973. Life history and feeding habits of the marine Nematode, Chromadora macrolaimoides Steiner. Oecologia 12: 303–314.

    Article  Google Scholar 

  • Tietjen, J. H. & J. J. Lee, 1977. Feeding behaviour of marine nematodes. In Coull, B. C. (ed.), Ecology of Marine Benthos. University of South Carolina Press, Columbia, USA: 21–36.

    Google Scholar 

  • Traunspurger, W., 1997. Bathymetric, seasonal and vertical distribution of feeding-types of nematodes in an oligotrophic lake. Vie et Milieu 47: 1–7.

    Google Scholar 

  • Traunspurger, W., 2000. The biology and ecology of lotic nematodes. Freshwater Biology 44: 29–45.

    Article  Google Scholar 

  • Traunspurger, W., 2002. Nematoda. In Rundle, S. D., A. L. Robertson & J. M. Schmid-Araya (eds), Freshwater Meiofauna: Biology and Ecology. Backhuys Publishers, Leiden: 63–104.

    Google Scholar 

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

    Article  Google Scholar 

  • Van Oevelen, D., K. Soetaert, J. J. Middelburg, P. M. J. Herman, L. Moodley, I. Hamels, T. Moens & C. H. R. Heip, 2006. Carbon flows through a benthic food web: Integrating biomass, isotope and tracer data. Journal of Marine Research 64: 453–482.

    Article  Google Scholar 

  • Warwick, R. M. & J. M. Gee, 1984. Community structure of estuarine meiobenthos. Marine Ecology Progress Series 18: 97–111.

    Article  Google Scholar 

  • Wright, S. W., S. W. Jeffrey, R. F. C. Mantoura, C. A. Llewellyn, T. Bjornland, D. Repeta & N. Welschmeyer, 1991. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Marine Ecology Progress Series 77: 183–196.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to S. Boyer, R. Fernandez and S. Gehner for their help in sample collection and preparation, and to two anonymous reviewers for their helpful comments. This study was funded by a national CNRS EC2CO-CYTRIX program. N. Majdi received a doctoral grant no. 31381-2008 by the French department of higher education and research (MESR).

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  1. EcoLab (Laboratoire Ecologie Fonctionnelle et Environnement), INP, UPS, Université de Toulouse, 118 route de Narbonne, 31062, Toulouse, France

    Nabil Majdi, Michèle Tackx & Evelyne Buffan-Dubau

  2. EcoLab, CNRS, 31062, Toulouse, France

    Nabil Majdi, Michèle Tackx & Evelyne Buffan-Dubau

  3. Department of Animal Ecology, University of Bielefeld, Morgenbreede 45, 33615, Bielefeld, Germany

    Walter Traunspurger

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  1. Nabil Majdi
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Majdi, N., Tackx, M., Traunspurger, W. et al. Feeding of biofilm-dwelling nematodes examined using HPLC-analysis of gut pigment contents. Hydrobiologia 680, 219–232 (2012). https://doi.org/10.1007/s10750-011-0920-0

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