Abstract
Non-native species are a major threat to aquatic ecosystems and the assessment of their invasiveness may be limited by the diverse ecological features needed to be accounted for. In this study, we combined complementary features of the autoecology and trophic ecology of Hemimysis anomala in a large deep lake (Lake Bourget) to assess its invasiveness. It was present in more than 80% of the 23 sites explored, indicating an extensive colonization of the lake. The mysid exhibited at least two generations per year, and the median individual growth rate was ~ 0.04 mg dry mass day−1 and ~ 0.09 mg dry mass day−1 for juveniles and adults, respectively. Consequently, the daily production for a typical reproductive swarm could reach more than 250 mg dry mass day−1 m−2 representing an important hotspot of secondary production. Individual measurements of stable carbon (δ13C) and nitrogen (δ15N) isotopes highlighted a trophic ontogenetic shift and indicated that subpopulations of H. anomala could mainly rely either on benthic or pelagic resources depending on the slope of the site. Because of its extensive colonization, its high growth rate, and trophic plasticity, H. anomala exhibits a high invasiveness and may strongly alter the food web of Lake Bourget.









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References
Adams, T. & R. Sterner, 2000. The effect of dietary nitrogen content on trophic level 15N enrichment. Limnology and Oceanography 45: 601–607.
Anderson, T., R. Stelzer, G. Drecktrah & S. Eggert, 2012. Secondary production of Chironomidae in a large eutrophic lake: implications for lake sturgeon production. Freshwater Science 31: 365–378.
Bade, D., S. Carpenter, J. Cole, P. Hanson & R. Hesslein, 2004. Controls of d13C-DIC in lakes: Geochemistry, lake metabolism, and morphometry. Limnology and Oceanography 49: 1160–1172.
Benke, A. C., 1998. Production dynamics of riverine chironomids: extremely high biomass turnover rates of primary consumers. Ecology 79: 899–910.
Borcherding, J., S. Murawski & H. Arndt, 2006. Population ecology, vertical migration and feeding of the Ponto-Caspian invader Hemimysis anomala in a gravel-pit lake connected to the River Rhine. Freshwater Biology 51: 2376–2387.
Borcherding, J., B. Hermasch & P. Murawski, 2007. Field observations and laboratory experiments on growth and lipid content of young-of-the-year perch. Ecology of Freshwater Fish 16: 198–209.
Brooking, T. E., L. G. Rudstam, S. D. Krueger, J. R. Jackson, A. B. Welsh & W. W. Fetzer, 2010. First occurrence of the mysid Hemimysis anomala in an inland lake in North America, Oneida Lake, NY. Journal of Great Lakes Research 36: 577–581.
Cucherousset, J. & J. Olden, 2011. Ecological impacts of non-native freshwater fishes. Fisheries 36: 215–230.
Cucherousset, J. & S. Villeger, 2015. Quantifying the multiple facets of isotopic diversity: new metrics for stable isotope ecology. Ecological Indicators 56: 152–160.
Daufresne, M., P. Bady & J.-F. Fruget, 2007. Impacts of global changes and extreme hydroclimatic events on macroinvertebrate community structures in the French Rhône River. Oecologia 151: 544–559.
Doi, H., K. Eisuke, T. Shigeto & S. Shuichi, 2007. Changes in carbon and nitrogen stable isotopes of chironomid larvae during growth, starvation and metamorphosis. Rapid Communications in Mass Spectrometry 21: 997–1002.
Dray, S. & A. B. Dufour, 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22: 1–20.
Dumont, S. & C. Muller, 2010. Distribution, ecology and impact of a small invasive shellfish, Hemimysis anomala in Alsatian water. Biological Invasions 12: 495–500.
Euclide, P. T., S. Hansson & J. D. Stockwell, 2017. Partial diel vertical migration in an omnivorous macroinvertebrate, Mysis diluviana. Hydrobiologia 787: 387–396.
France, R. L., 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnology and Oceanography 40: 1310–1313.
Gannes, L., C. M. del Rio & P. Koch, 1998. Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology 119A: 725–737.
Golaz, F. & R. Vainola, 2013. Répartition, dynamique saisonnière et analyse de l’ADN mitochondrial du crustacé mysidé invasif Hemimysis anomala G.O. Sars 1907 dans le Léman. Bulletin de la Société Vaudoise des Sciences Naturelles 93: 101–117.
Harris, D., W. Horwarth & C. van Kessel, 2001. Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon-13 isotopic analysis. Soil Science Society of America Journal 65: 1853–1856.
Hershey, A. E., S. Beaty, K. Fortino, S. Kelly, M. Keyse, C. Luecke, W. J. O’Brien & C. Whalen, 2006. Stable isotope signatures of benthic invertebrates in arctic lakes indicate limited coupling to pelagic production. Limnology and Oceanography 51: 177–188.
Jackson, A., R. Inger, A. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.
Jazdzewski, K., 1980. Range extensions of some gammaridean species in European inland waters caused by human activity. Crustaceana 6: 84–107.
Kamenova, S., T. J. Bartley, D. A. Bohan, J. R. Boutain, R. I. Colautti, I. Domaizon, C. Fontaine, A. Lemainque, I. Le Viol, G. Mollot, M. E. Perga, V. Ravigné & F. Massol, 2017. Invasions toolkit: current methods for tracking the spread and impact of invasive species. In David, A., A. J. D. Bohan & M. François (eds), Advances in Ecological Research. Academic Press, London: 85–182.
Ketelaars, H. M., F. Lambregts-van de Clundert, C. Carpentier, A. Wagenvoort & W. Hoogenboezem, 1999. Ecological effects of the mass occurrence of the Ponto-Caspian invader, Hemimysis anomala G.O. Sars, 1907 (Crustacea: Mysidacea), in a freshwater storage reservoir in the Netherlands, with notes on its autecology and new records. Hydrobiologia 394: 233–248.
Kuns, M. & W. Sprules, 2000. Zooplankton production in Lake Ontario: A multistrata approach. Canadian Journal of Fisheries and Aquatic Sciences 57: 2240–2247.
Koops, M., J. Gerlofsma & J. Marty, 2010. Risk assessment of the bloody red shrimp (Hemimysis anomala). Canadian Science Advisory Secretariat Doc. 2009(107): 20.
Layman, C., A. Arrington, C. Montana & D. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.
Leoni, B., 2017. Zooplankton predators and preys: body size and stable isotope to investigate the pelagic food web in a deep lake (Lake Iseo, Northern Italy). Journal of Limnology. 76: 85–93.
Macneil, C., P. Boets, K. Lock & P. L. M. Goethals, 2013. Potential effects of the invasive ‘killer shrimp’ (Dikerogammarus villosus) on macroinvertebrate assemblages and biomonitoring indices. Freshwater Biology 58: 171–182.
Marty, J., 2007. Biological synopsis of the bloody red shrimp (Hemimysis anomala) Fisheries and Oceans Canada; Great Lakes Laboratory for Fisheries and Aquatic Sciences, 45.
Marty, J. & D. Planas, 2008. A comparison of methods to determine algal δ13C in freshwater. Limnology and Oceanography Methods 6: 51–63.
Marty, J., K. Bowen, M. Koops & M. Power, 2010. Distribution and ecology of Hemimysis anomala, the latest invader of the Great Lakes basin. Hydrobiologia 647: 71–80.
Marty, J., J. Ives, Y. de Lafontaine, S.-P. Despatie, M. Koops & M. Power, 2012. Evaluation of carbon pathways supporting the diet of invasive Hemimysis anomala in a large river. Journal of Great Lakes Research 38: 45–51.
McCutchan, J., W. Lewis, K. Kendall & C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.
McDowell, W. G., W. H. McDowell & J. E. Byers, 2016. Mass mortality of a dominant invasive species in response to an extreme climate event: implications for ecosystem function. Limnology and Oceanography 65: 177–188.
Miquet, A., 1997. Regulation of the lac du Bourget (French Alps): environmental impact of new management rules. Revue de géographie alpine 85: 11–21.
Novais, A., D. Batista, F. Cássio, C. Pascoal & R. Sousa, 2017. Effects of invasive clam (Corbicula fluminea) die-offs on the structure and functioning of freshwater ecosystems. Freshwater Biology 62: 1908–1916.
Ogonowski, M., J. Duberg, S. Hansson & E. Gorokhova, 2013. Behavioral, ecological and genetic differentiation in an open environment – a study of a mysid population in the Baltic sea. PLoS ONE 8: e57210.
Ozersky, T., D. O. Evans & B. K. Ginn, 2015. Invasive mussels modify the cycling, storage and distribution of nutrients and carbon in a large lake. Freshwater Biology 60: 827–843.
Parnell, A. & A. Jackson, 2013. Siar: Stable Isotope Analysis in R: R package version 4.2. https://CRAN.R-project.org/package=siar.
Parnell, A., R. Inger, S. Bearhop & A. Jackson, 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5: 1–5.
Parnell, A., D. Phillips, S. Bearhop, B. Semmens, E. Ward, J. Moore, A. Jackson & R. Inger, 2012. Bayesian Stable Isotope Mixing Models. Evironmetrics, eprint arXiv:1209.6457.
Phillips, D., 2001. Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127: 166–170.
Quantum GIS Development Team, 2017. Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
R Development Core Team, 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/.
Ricciardi, A., S. Avlijas & J. Marty, 2011. Forecasting the ecological impacts of the Hemimysis anomala invasion in North America: lessons from other freshwater mysid introductions. Journal of Great Lakes Research 38: 7–13.
Salemaa, H. & V. Hietalahti, 1993. Hemimysis anomala G.O. Sars (Crustacea: Mysidacea) – Immigration of a Pontocaspian mysid into the Baltic Sea. Annales Zoologici Fennici 30: 271–276.
Stephenson, J. M., G. Carr, U. Gruenert & A. Morin, 2007. Evaluation of two timesaving techniques for processing benthic invertebrate samples for estimating secondary production. Journal of the North American Benthological Society 26: 611–619.
Syvaranta, J. & M. Rautio, 2010. Zooplankton, lipids and stable isotopes: importance of seasonal, latitudinal, and taxonomic differences. Canadian Journal of Fisheries and Aquatic Sciences 67: 1721–1729.
Tachet, H., P. Richoux, M. Bournaud & P. Usseglio-Polatera, 2010. Invertébrés d’eau douce – Systématique, biologie, écologie. 3rd edn. CNRS Editions, Paris.
Vander Zanden, J. & Y. Vadeboncoeur, 2002. Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83: 2152–2161.
Vander Zanden, J., M. Casselman & J. Rasmussen, 1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401: 464–467.
Walsh, J. R., S. R. Carpenter & M. J. Vander Zanden, 2016. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proceedings of the National Academy of Sciences USA 113: 4081–4085.
Walsh, M. G., B. F. Lantry, B. Boscarino, K. Bowen, J. Gerlofsma, T. Schaner, R. Back, J. Questel, A. G. Smythe, R. Cap, M. Goehle, B. Young, M. Chalupnicki, J. H. Johnson & J. E. McKenna, 2010. Early observations on an emerging Great Lakes invader Hemimysis anomala in Lake Ontario. Journal of Great Lakes Research 36: 499–504.
Wetzel, R. G., 2001. Limnology. Lake and River Ecosystems, 3rd ed. Academic Press, London.
Wittmann, K. J., 2007. Continued massive invasion of Mysidae in the Rhine and Danube river systems, with first records of the order Mysidacea (Crustacea: Malacostraca: Peracarida) for Switzerland. Revue Suisse de Zoologie 114: 65–86.
Wittmann, K. & A. Ariani, 2009. Reappraisal and range extension of non-indigenous Mysidae (Crustacea, Mysida) in continental and coastal waters of eastern France. Biological Invasions 11: 401–407.
Acknowledgements
We are indebted to Katya Kovalenko, Luigi Naselli-Flores, as well as three anonymous reviewers for their valuable comments that greatly improved early versions of the manuscript. We also would like to thank the Université de Savoie Mont-Blanc for the financial support of this study through the “BIB” project. We are grateful to Dominique Picard and the Club de Plongée de Chambéry (GSRL) for assistance in the search for H. anomala during diving explorations, as well as to Marie Rosières and Jean-Noël Avrillier for their support in conditioning H. anomala for the analyses of stable isotopes and individual measurements.
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Frossard, V., Fontvieille, D. What is the invasiveness of Hemimysis anomala (Crustacea, Mysidae) in the large deep Lake Bourget, France?. Hydrobiologia 814, 219–232 (2018). https://doi.org/10.1007/s10750-018-3538-7
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DOI: https://doi.org/10.1007/s10750-018-3538-7


