Potential role of fungi in plankton food web functioning and stability: a simulation analysis based on Lake Biwa inverse model
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Recent investigations of molecular diversity in the plankton of lakes and coastal lagoons have detected an unexpected diversity of fungi including chytrids. Microscopic observations have provided evidence for the presence of two main forms. The sporangia are implied in algal parasitism. The propagules, i.e. uniflagellated zoospores, may constitute an alternate resource for consumers. These results suggest a need to reconsider the concept of plankton food web functioning. In order to describe the potential role of fungi in food web functioning, we revisit the model of carbon flows in the photic zone of the North basin of Lake Biwa in summer, established using the inverse analysis method for estimating missing flow values. In the absence of quantification of the flows induced by fungal activity, simulations are realised of their potential role in the plankton food web. Different rates of parasitism of micro-phytoplankton are tested, with a return of this carbon to the consumer via the consumption of zoospores by mesozooplankton and, at a lower rate, microzooplankton. The presence of this indirect pathway channelling micro-phytoplankton production to the consumers via the fungi, leads to the following trends: (i) an enhancement of the trophic efficiency index, (ii) a decrease of the ratio detritivory/herbivory, (iii) a decrease of the percentage of carbon flowing in cyclic pathways, and (iv) an increase in the relative ascendency of the system. Relative ascendency, which indicates pathways more specialised and less redundant, is related to theories linking food web patterns and stability. A high ascendency in the plankton food web (low trophic level), if connected to a food web of high redundancy at higher trophic levels (e.g. nekton food web) would fit well to the stabilising pattern called structural asymmetry, considered a stability criterion. More precise models, taking into account the species diversity of fungi and the high specificity of their parasitism on the micro-phytoplankton, would further accentuate this observation.
KeywordsFood web Parasites Plankton Inverse model Ecological network analysis
The authors thank the DREP project from the French ANR program for financial support of this study, George A Jackson for providing the source Matlab© program, Robert E Ulanowicz for the Netwrk 4.2 program used, the 2 anonymous reviewers for their useful remarks and Galen A. Johnson for correcting English.
- Kagami, M., B. W. Ibelings, A. de Bruin & E. Van Donk, 2005. Vulnerability of Asterionella Formosa to Daphnia grazing: the impact of a fungal parasite. Verhandlungen: Internationale Vereinigung fur Theoretische und Angewandte Limnologie 29: 350–354.Google Scholar
- Kagami, M., E. Von Elert, B. W. Ibelings, A. De Bruin & E. Van Donk, 2007b. The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proceedings of the Royal Society B: Biological Sciences 274: 1561–1566.CrossRefPubMedGoogle Scholar
- Kay, J. J., L. A. Graham & R. E. Ulanowicz, 1989. A detailed guide to network analysis. In Wulff, F., J. G. Field & K. H. Mann (eds), Network Analysis in Marine Ecology: Methods and Applications. Springer-Verlag, Heidelberg: 15–61.Google Scholar
- Lafferty, K. D., S. Allesina, M. Arim, C. J. Briggs, G. DeLeo, A. P. Dobson, J. A. Dunne, P. T. Johnson, A. M. Kuris, D. J. Marcogliese, N. D. Martinez, J. Memmott, P. A. Marquet, J. P. McLaughlin, E. A. Mordecai, M. Pascual, R. Poulin & D. W. Thieltges, 2008. Parasites in food webs: the ultimate missing links. Ecology Letters 11: 533–546.CrossRefPubMedGoogle Scholar
- Lefèvre, E., C. Bardot, C. Noël, J. F. Carrias, E. Viscogliosi, C. Amblard & T. Sime-Ngando, 2007. Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environmental Microbiology 9: 61–71.CrossRefPubMedGoogle Scholar
- Lefèvre, E., B. Roussel, C. Amblard & T. Sime-Ngando, 2008. The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS ONE 3.Google Scholar
- Legendre, L. & F. Rassoulzadegan, 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41: 153–172.Google Scholar
- Nakanishi, M., Y. Tezuka, T. Narita, O. Mitamura, K. Kawabata & S.-I. Nakano, 1992. Phytoplankton primary production and its fate in a pelagic area of Lake Biwa. Archiv für Hydrobiologie Beiheft Ergebnisse der Limnologie 35: 47–67.Google Scholar
- Pratt, J. R. & J. Cairns, 1985. Functional groups in the protozoa: roles in differing ecosystems. J Protozool 32: 415–423.Google Scholar
- Ulanowicz, R. E., 1986. Growth & Development: Ecosystems Phenomenology. Springer-Verlag, New York: 203.Google Scholar
- Ulanowicz, R. E., 1997. Ecology, The Ascendent Perspective. Columbia University Press, New York: 201 pp.Google Scholar
- Ulanowicz, R. E., 1999. NETWRK 4.2 a Package of Computer Algorithms to Analyse Ecological Flow Networks. http://www.cbl.umces.edu/~ulan/ntwk/network.html.
- Urabe, J., K. Kawabata, M. Nakanishi & K. Shimizu, 1996. Grazing and food size selection of zooplankton community in Lake Biwa during BITEX ‘93. Japanese Journal of Limnology 57: 27–37.Google Scholar
- Van den Meersche, K., K. Soetaert & D. Van Oevelen, 2009. xsample(): An R Function for Sampling Linear Inverse Problems. Journal of Statistical Software 30: code snippet 1.Google Scholar