Abstract
Submerged aquatic vegetation (SAV) plays important roles in shallow lakes. In addition to its refuge effect for zooplankton, one key role of SAV is to provide diverse ecological niches to these organisms. The reduction of habitat complexity due to loss of SAV might thus have huge effects on zooplankton communities. The objective of this study was to investigate the relationship between SAV abundance and composition and zooplankton functional diversity and community structure. We used as model system the littoral zone of Lake St. Pierre (Québec, Canada), a shallow fluvial lake experiencing dramatic changes in SAV cover. Our sampling protocol allowed us to analyse the relationship between SAV and zooplankton along a gradient of SAV abundance. We showed that SAV abundance explained 41% of the variation in the zooplankton community structure and 25% of the variation in zooplankton functional diversity. Our results also indicated that the presence of the benthic cyanobacterium Gloeotrichia sp. in SAV beds had a structuring effect within the dominant family of Chydoridae, being negatively correlated to the abundance of relatively large-bodied species. Our findings suggest that loss in SAV biomass and complexity can affect both community structure and functional diversity of zooplankton in shallow fluvial lakes.
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References
Adamczuk, M., 2014. Niche separation by littoral-benthic Chydoridae (Cladocera, Crustacea) in a deep lake – potential drivers of their distribution and role in littoral-pelagic coupling. Journal of Limnology 73: 490–501.
Amoros, C., 1984. Introduction pratique à la systématique des eaux continentales françaises. 5. Crustacés Cladocères. Association française de Limnologie, Paris.
Barnett, A. & B. E. Beisner, 2007. Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88(7): 1675–1686.
Barnett, A. J., K. Finlay & B. E. Beisner, 2007. Functional diversity of crustacean zooplankton communities: towards a trait-based classification. Freshwater Biology 52(5): 796–813.
Basu, B. K., J. Kalff & B. Pinel-Alloul, 2000. The influence of macrophyte beds on plankton communities and their export from fluvial lakes in the St Lawrence River. Freshwater Biology 45(4): 373–382.
Bergmann, M. & R. H. Peters, 1980. A simple reflectance method for the measurement of particulate pigment in Lake Water and its application to phosphorus–chlorophyll–Seston relationships. Canadian Journal of Fisheries and Aquatic Sciences 37(1): 111–114.
Blanchet, F. G., P. Legendre & D. Borcard, 2008a. Forward selection of explanatory variables. Ecology 89(9): 2623–2632.
Blanchet, F. G., P. Legendre & D. Borcard, 2008b. Modelling directional spatial processes in ecological data. Ecological Modelling 215(4): 325–336.
Blindow, I., 1992. Decline of charophytes during eutrophication: comparison with angiosperms. Freshwater Biology 28(1): 9–14.
Borcard, D., F. Gillet & P. Legendre, 2011. Numerical ecology with R. Springer Science & Business Media, New York.
Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73(3): 1045–1055.
Bottrell, H. H., A. Duncan, Z. Gliwicz, A. Herzig-Grygierek, A. Hillbricht-Illowska, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norwegian Journal of Zoology 24: 419–456.
Brucet, S., D. Boix, S. Gascón, J. Sala, X. D. Quintana, A. Badosa, M. Søndergaard, T. L. Lauridsen & E. Jeppesen, 2009. Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: north temperate Denmark and Mediterranean Catalonia (Spain). Ecography 32: 692–702.
Burks, R. L., D. M. Lodge, E. Jeppesen & T. L. Lauridsen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47(3): 343–365.
Castro, B. B., S. M. Marques & F. Gonçalves, 2007. Habitat selection and diel distribution of the crustacean zooplankton from a shallow Mediterranean lake during the turbid and clear water phases. Freshwater Biology 52(3): 421–433.
Chullasorn, S., W.-X. Yang, H.-U. Dahms, P. Kangtia, M. Holynska, W. Anansatitporn, L. O. Sanoamuang & J.-S. Hwang, 2009. Naupliar development of Eucyclops cf. serrulatus tropicalis, Eucyclops. cf. spatulatus, and Ectocyclops medius Kiefer, 1930 (Copepoda: Cyclopidae). Zoological Studies 48(1): 12–32.
Cuthbert, I. D. & P. Del Giorgio, 1992. Toward a standard method of measuring color in freshwater. Limnology and Oceanography 37(6): 1319–1326.
D’Arcy, P. & R. Carignan, 1997. Influence of catchment topography on water chemistry in southeastern Quebec Shield lakes. Canadian Journal of Fisheries and Aquatic Sciences 54(10): 2215–2227.
Declerck, S., M. Vanderstukken, A. Pals, K. Muylaert & L. de Meester, 2007. Plankton biodiversity along a gradient of productivity and its mediation by macrophytes. Ecology 88(9): 2199–2210.
Drenner, R. & S. McComas, 1980. The roles of zooplankter escape ability and fish size selectivity in the selective feeding and impact of planktivorous fish. Evolution and Ecology of Zooplankton Communities 587: 593.
Edmonston, W. T., 1959. Fresh-Water Biology. Wiley, New York.
Fey, S. B., Z. A. Mayer, S. C. Davis & K. L. Cottingham, 2010. Zooplankton grazing of Gloeotrichia echinulata and associated life history consequences. Journal of Plankton Research 32(9): 1337–1347.
Gonzàlez Sagrario, M. A. & E. Balseiro, 2010. The role of macroinvertebrates and fish in regulating the provision by macrophytes of refugia for zooplankton in a warm temperate shallow lake. Freshwater Biology 55: 2133–2166.
Gyllström, M. & L.-A. Hansson, 2004. Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquatic Sciences 66(3): 274–295.
Haney, J. F. & al., 2010. An-Image-Based Key to the Zooplankton of the Northeast, USA, version 4.0 released 2010. University of New Hampshire Center for Freshwater Biology.
Havens, K., 2008. Cyanobacteria blooms: effects on aquatic ecosystems. Chap. 33. Harmful Algal Blooms: State of the Science and Research Needs. Advances in Experimental and Medicine Biology 619: 733–747.
Hebert, P. D. N., 1995. The Daphnia of North America: An Illustrated Fauna. University of Guelph, CD-ROM.
Heck Jr, K. L. & L. B. Crowder, 1991. Habitat structure and predator –prey interactions in vegetated aquatic systems. In Bell, S. E., S. Bell, E. McCoy & H. Mushinsky (eds), Habitat Structure. Population and Community Biology Series, Vol. 8. Springer, Dordrecht: 281–299.
Horppila, J. & L. Nurminen, 2003. Effects of submerged macrophytes on sediment resuspension and internal phosphorus loading in Lake Hiidenvesi (southern Finland). Water Research 37(18): 4468–4474.
Hudon, C., M. De Seve & A. Cattaneo, 2014. Increasing occurrence of the benthic filamentous cyanobacterium Lyngbya wollei: a symptom of freshwater ecosystem degradation. Freshwater Science 33(2): 606–618.
Hudson, P. L. & L. T. Lesko, 2003. Free-living and Parasitic Copepods of the Laurentian Great Lakes: Keys and Details on Individuals Species. Great Lakes Science Center Home Page, Ann Arbor, MI.
Jean, M., & G. Létourneau, 2014. Freshwater Wetlands, Third Edition. St. Lawrence Action Plan, Monitoring the State of the St. Lawrence [available from http://plantstlaurent.qc.ca/en/state_monitoring/monitoring_sheets/monitoring_the_state_of_the_st_lawrence_river.html#c2411].
Jeppesen, E., et al., 2012. The Structuring Role of Submerged Macrophytes in Lakes, Vol. 131. Springer Science & Business Media, New York.
Jeppesen, E., J. Jensen, M. Søndergaard, T. Lauridsen, L. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342–343: 151–164.
Jongman, R. H., C. J. Ter Braak & O. F. Van Tongeren, 1995. Data Analysis in Community and Landscape Ecology, Vol. 2. Cambridge University Press, Cambridge.
Kelaher, B. P. & J. C. Castilla, 2005. Habitat characteristics influence macrofaunal communities in coralline turf more than mesoscale coastal upwelling on the coast of Northern Chile. Estuarine Coastal and Shelf Science 63(1–2): 155–165.
Körner, S., 2002. Loss of submerged macrophytes in shallow lakes in North-Eastern Germany. International Review of Hydrobiology 87(4): 375–384.
Laliberté, E. & P. Legendre, 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1): 299–305.
Laliberté, E., Legendre, P. & B. Shipley, 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12.
Lauridsen, T. L., L. J. Pedersen, E. Jeppesen & M. Sondergaard, 1996. The importance of macrophyte bed size for cladoceran composition and horizontal migration in a shallow lake. Journal of Plankton Research 18(12): 2283–2294.
Laviolette, N., D. Fournier, P. Dumont & Y. Mailhot, 2003. Caractérisation des communautés de poissons et développement d’un indice d’intégrité biotique pour le fleuve Saint-Laurent, 1995-1997. Société de la faune et des parcs du Québec, Direction de la recherche sur la faune, Québec.
Legendre, P. & M. J. Fortin, 1989. Spatial pattern and ecological analysis. Vegetatio 80(2): 107–138.
Legendre, P. & E. D. Gallagher, 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129(2): 271–280.
Lévesque, D., A. Cattaneo, C. Hudon & P. Gagnon, 2012. Predicting the risk of proliferation of the benthic cyanobacterium Lyngbya wollei in the St. Lawrence River. Canadian Journal of Fisheries and Aquatic Sciences 69(10): 1585–1595.
Lorenzen, C. J., 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnology and Oceanography 12(2): 343–346.
Madsen, J. D., P. A. Chambers, W. F. James, E. W. Koch & D. F. Westlake, 2001. The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444: 71–84.
Malley, D. F., S. G Lawrence, M. A. MacIver & W. J. Findlay, 1989. Range of variation in estimates of dry weight for planktonic crustacea and rotifera from temperate North American lakes. Canadian Technical Report of Fisheries and Aquatic Sciences no. 1666, Central and Arctic Region, Department of Fisheries and Oceans, Winnipeg, Manitoba.
Masclaux, H., G. Bourdier, L. Jouve, E. Duffaud & A. Bec, 2014. Temporal changes in essential fatty acid availability in different food sources in the littoral macrophyte zone. Hydrobiologia 736(1): 127–137.
Massicotte, P., J.-J. Frenette, R. Proulx, B. Pinel-Alloul & A. Bertolo, 2014. Riverscape heterogeneity explains spatial variation in zooplankton functional evenness and biomass in a large river ecosystem. Landscape Ecology 29(1): 67–79.
Masson, S., B. Pinel-Alloul, G. Methot & N. Richard, 2004. Comparison of nets and pump sampling gears to assess zooplankton vertical distribution in stratified lakes. Journal of Plankton Research 26(10): 1199–1206.
Matias, M. G., A. J. Underwood, D. F. Hochuli & R. A. Coleman, 2010. Independent effects of patch size and structural complexity on diversity of benthic macroinvertebrates. Ecology 91(7): 1908–1915.
Meerhoff, M., C. Iglesias, F. T. De Mello, J. M. Clemente, E. Jensen, T. L. Lauridsen & E. Jeppesen, 2007. Effects of habitat complexity on community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biology 52(6): 1009–1021.
Mouchet, M. A., S. Villeger, N. W. H. Mason & D. Mouillot, 2010. Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Functional Ecology 24(4): 867–876.
Oksanen, J., 2013. Multivariate Analysis of Ecological Communities in R: Vegan Tutorial. University Oulu, Finland.
Pakeman, R. J., 2011. Functional diversity indices reveal the impacts of land use intensification on plant community assembly. Journal of Ecology 99(5): 1143–1151.
Pennak, R. W., 1957. Species composition of limnetic zooplankton communities. Limnology and Oceanography 2(3): 222–232.
Pinel-Alloul, B., E. Cusson & L. Aldamman, 2011. Diversity and spatial distribution of copepods in the St. Lawrence River (Québec, Canada). Crustaceana Monographs 16: 425–429.
Prepas, E., 1978. Sugar-frosted Daphnia: an improved fixation technique for Cladocera. Limnology and Oceanography 23(3): 557–559.
R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org/].
Reid, J. W. & C. E. Williamson, 2010. Copepoda. In Thorp, J. H. & A. P. Covich (eds), Ecology and Classification of North American Freshwater Invertebrates. Elsevier Inc., Amsterdam: 829–899.
Sakuma, M., T. Hanazato, A. Saji & R. Nakazato, 2004. Migration from plant to plant: an important factor controlling densities of the epiphytic cladoceran Alona (Chydoridae, Anomopoda) on lake vegetation. Limnology 5(1): 17–23.
Scheffer, M., S. Hosper, M. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8(8): 275–279.
Scheffer, M., 2004. Ecology of Shallow Lakes. Springer Science & Business Media, New York.
Smith, K. & C. H. Fernando, 1978. A Guide to Freshwater Calanoid and Cyclopoid Copepod Crustacea of Ontario. University of Waterloo Biology Series, Waterloo.
Tall, L., A. Armellin, B. Pinel-Alloul, G. Méthot & C. Hudon, 2015. Effects of hydrological regime, landscape features, and environment on macroinvertebrates in St. Lawrence River wetlands. Hydrobiologia. doi:10.1007/s10750-015-2531-7.
Timms, R. M. & B. Moss, 1984. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland ecosystem. Limnology and Oceanography 29(3): 472–486.
Tourville Poirier, A. M., A. Cattaneo & C. Hudon, 2010. Benthic cyanobacteria and filamentous chlorophytes affect macroinvertebrate assemblages in a large fluvial lake. Journal of the North American Benthological Society 29(737): 749.
Van Onsem, S., S. De Backer & L. Triest, 2010. Microhabitat-zooplankton relationship in extensive macrophyte vegetations of eutrophic clear-water ponds. Hydrobiologia 656(1): 67–81.
Vermaire, J. C., Y. T. Prairie & I. Gregory-Eaves, 2012. Diatom-inferred decline of macrophyte abundance in lakes of southern Quebec, Canada. Canadian Journal of Fisheries and Aquatic Sciences 69(3): 511–524.
Villeger, S., N. W. H. Mason & D. Mouillot, 2008. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89(8): 2290–2301.
Walseng, B., D. O. Hessen, G. Halvorsen & A. K. Schartau, 2006. Major contribution from littoral crustaceans to zooplankton species richness in lakes. Limnology and Oceanography 51(6): 2600–2606.
Willis, S. C., K. O. Winemiller & H. Lopez-Fernandez, 2005. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia 142(2): 284–295.
Yin, Y., J. S. Winkelman & H. A. Langrehr, 2000. Long term resource monitoring program procedures: aquatic vegetation monitoring. US Geological Survey, Upper Midwest Environmental Sciences Center, La Crosse.
Acknowledgments
We would like to thank Ginette Méthot and Myriam Boisvert for their technical assistance for zooplankton identification. We also thank Philippe Massicotte, Raphaël Proulx and Guillaume Rheault for discussion about the experimental design and the statistical analysis. We also thank Captain Alain Ledoux for safely driving our team on the lake and the members of Jean-Jacques Frenette and Simon Bélanger laboratories who have helped during the sampling campaign as well as Christiane Hudon’s team members who collected SAV data. Financial support was provided by the Fond Québécois de la Recherche Nature et Technologie (ISI-FQRNT), the RIVE-UQTR research centre, and the Groupe de Recherche Interuniversitaire en Limnologie et en environnement aquatique (GRIL), who also made possible data sharing between the researchers. Thanks to Morgan Botrel for the coordination during sampling and laboratory analysis. Finally, we thank the three reviewers and Mariana Meerhoff, associate editor, for their useful and constructive comments that help us improve significantly this paper.
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Guest editors: M. Beklioğlu, M. Meerhoff, T. A. Davidson, K. A. Ger, K. E. Havens & B. Moss / Shallow Lakes in a Fast Changing World
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Bolduc, P., Bertolo, A. & Pinel-Alloul, B. Does submerged aquatic vegetation shape zooplankton community structure and functional diversity? A test with a shallow fluvial lake system. Hydrobiologia 778, 151–165 (2016). https://doi.org/10.1007/s10750-016-2663-4
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DOI: https://doi.org/10.1007/s10750-016-2663-4