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Spatial aggregation of native with non-native freshwater bivalves and activity depletion under summer heat waves: ‘dangerous liaisons’ in a climate change context

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Abstract

Freshwater mussels are considered sedentary organisms. However, their foot provides the organ of locomotion, which enables an active behaviour. Their behaviour includes righting, horizontal movements and burrowing into the substrate. The objective of this study was to analyse the influence of non-native (Corbicula fluminea) competitors on the pedal activity of native (Unio delphinus) freshwater mussels in a climate change context. The pedal activity was scored and compared among different species compositions, population density and exposure to heat wave progression. The results showed a significant effect of species composition and heat wave progression. In addition, a significant effect of species composition × population density was found. Mussels at low density conditions exposed to dense aggregations of C. fluminea showed lower pedal activity than individuals in intraspecific treatments, or individuals at high density conditions exposed to low densities of C. fluminea. Maximum pedal activity was recorded at the thermal peak. After that, pedal activity was reduced when high temperature was maintained over time. Altogether, present results suggest that lower pedal activity at high C. fluminea densities may expose mussels to more intense interspecific competition. In addition, heat waves may compromise mussels’ ability to locate refuge areas in front of receding waters.

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References

  • Allen, D. C. & C. C. Vaughn, 2009. Burrowing behavior of freshwater mussels in experimentally manipulated communities. Journal of the North American Benthological Society 28: 93–100.

    Article  Google Scholar 

  • Amyot, J. P. & J. Downing, 1997. Seasonal variation in vertical and horizontal movement of the freshwater bivalve Elliptio complanata (Mollusca: Unionidae). Freshwater Biology 37: 345–354.

    Article  Google Scholar 

  • Amyot, J. P. & J. A. Downing, 1998. Locomotion in Elliptio complanata (Mollusca: Unionidae): a reproductive function? Freshwater Biology 39: 351–358.

    Article  Google Scholar 

  • Anthony, J. L. & J. A. Downing, 2001. Exploitation trajectory of a declining fauna: a century of freshwater mussel fisheries in North America. Canadian Journal of Fisheries and Aquatic Sciences 58: 2071–2090.

    Article  Google Scholar 

  • Araujo, R., 2011. Unio delphinus. In IUCN Red List of Threatened Species. Version 2015.3. http://www.iucnredlist.org/. Accessed 12 June 2018.

  • Archambault, J. M., W. G. Cope & T. J. Kwak, 2013. Burrowing, byssus, and biomarkers: behavioral and physiological indicators of sublethal thermal stress in freshwater mussels (Unionidae). Marine and Freshwater Behaviour and Physiology 46: 229–250.

    Article  CAS  Google Scholar 

  • Bogan, A. E., 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595: 139–147.

    Article  Google Scholar 

  • Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. H. Stevens & J. S. S. White, 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24: 127–135.

    Article  Google Scholar 

  • Cambray, J. A., 2003. Impact on indigenous species biodiversity caused by the globalization of alien recreational freshwater fisheries. Hydrobiologia 500: 217–230.

    Article  Google Scholar 

  • Cardinale, B. J., M. A. Palmer & S. L. Collins, 2002. Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415: 426–429.

    Article  CAS  Google Scholar 

  • Crespo, D., M. Dolbeth, S. Leston, R. Sousa & M. A. Pardal, 2015. Distribution of Corbicula fluminea in the invaded range: a geographic approach with notes on species traits variability. Biological Invasions 17: 2087–2101.

    Article  Google Scholar 

  • Dong, Y., L. P. Miller, J. G. Sanders & G. N. Somero, 2008. Heat-shock protein 70 (hsp70) expression in four limpets of the Genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress. Biological Bulletin 215: 173–181.

    Article  Google Scholar 

  • Downing, J. A., Y. Rochon, M. Pérusse & H. Harvey, 1993. Spatial aggregation, body size, and reproductive success in the freshwater mussel Elliptio complanata. Journal of the North American Benthological Society 12: 148–156.

    Article  Google Scholar 

  • Ferreira-Rodríguez, N. & I. Pardo, 2017. The interactive effects of temperature, trophic status and the presence of an exotic clam on the performance of a native freshwater mussel. Hydrobiologia 797: 171–182.

    Article  Google Scholar 

  • Ferreira-Rodríguez, N., I. Fernández, M. L. Cancela & I. Pardo, 2018a. Multibiomarker response shows how native and non-native freshwater bivalves differentially cope with heat wave events. Aquatic Conservation: Marine and Freshwater Ecosystems 28: 934–943.

    Article  Google Scholar 

  • Ferreira-Rodríguez, N., R. Sousa & I. Pardo, 2018b. Negative effects of Corbicula fluminea over native freshwater mussels. Hydrobiologia 810: 85–95.

    Article  Google Scholar 

  • Feyen, L. & R. Dankers, 2009. Impact of global warming on stream flow drought in Europe. Journal of Geophysical Research: Atmospheres. https://doi.org/10.1029/2008JD011438.

    Article  Google Scholar 

  • Froufe, E., D. V. Gonçalves, A. Teixeira, R. Sousa, S. Varandas, M. Ghamizi, A. Zieritz & M. Lopes-Lima, 2016. Who lives where? Molecular and morphometric analyses clarify which Unio species (Unionida, Mollusca) inhabit the southwestern Palearctic. Organisms Diversity and Evolution 16: 597–611.

    Article  Google Scholar 

  • Gallardo, B. & D. C. Aldridge, 2013. Evaluating the combined threat of climate change and biological invasions on endangered species. Biological Conservation 160: 225–233.

    Article  Google Scholar 

  • Gama, M., D. Crespo, M. Dolbeth & P. M. Anastácio, 2017. Ensemble forecasting of Corbicula fluminea worldwide distribution: projections of the impact of climate change. Aquatic Conservation: Marine and Freshwater Ecosystems 27: 675–684.

    Article  Google Scholar 

  • Ganser, A. M., T. J. Newton & R. J. Haro, 2015. Effects of elevated water temperature on physiological responses in adult freshwater mussels. Freshwater Biology 60: 1705–1716.

    Article  Google Scholar 

  • Gillis, P. L., 2012. Cumulative impacts of urban runoff and municipal wastewater effluents on wild freshwater mussels (Lasmigona costata). Science of The Total Environment 431: 348–356.

    Article  CAS  Google Scholar 

  • Gough, H. M., A. M. G. Landis & J. A. Stoeckel, 2012. Behaviour and physiology are linked in the responses of freshwater mussels to drought. Freshwater Biology 57: 2356–2366.

    Article  Google Scholar 

  • Haag, W. R., 2012. North American freshwater mussels: natural history, ecology, and conservation. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Howard, J. K. & K. M. Cuffey, 2003. Freshwater mussels in a California North Coast Range river: occurrence, distribution, and controls. Journal of the North American Benthological Society 22: 63–77.

    Article  Google Scholar 

  • IBM SPSS Statistics for Windows, 2010. Version 19.0. IBM Corp, Armonk.

  • IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Intergovernmental Panel on Climate Change, Geneva.

  • IUCN, 2019. The IUCN Red List of Threatened Species. Version 2018-2. Available at http://www.iucnredlist.org/. Accessed 04Feb 2019.

  • Jeschke, J. M. & D. L. Strayer, 2005. Invasion success of vertebrates in Europe and North America. Proceedings of the National Academy of Sciences 102: 7198–7202.

    Article  CAS  Google Scholar 

  • Jones, P. D., 1988. Hemispheric surface air temperature variations: recent trends and an update to 1987. Journal of Climate 1: 654–660.

    Article  Google Scholar 

  • Keiser, C. N., C. M. Wright, N. Singh, J. A. DeShane, A. P. Modlmeier & J. N. Pruitt, 2015. Cross-fostering by foreign conspecific queens and slave-making workers influences individual-and colony-level personality. Behavioral Ecology and Sociobiology 69: 395–405.

    Article  Google Scholar 

  • Lopes-Lima, M., R. Sousa, J. Geist, D. C. Aldridge, R. Araujo, J. Bergengren, Y. Bespalaya, E. Bódis, L. Burlakova, D. van Damme, K. Douda, E. Froufe, D. Georgiev, C. Gumpinger, A. Karatayev, U. Kebapci, I. Killeen, J. Lajtner, B. Larsen, R. Lauceri, A. Legakis, S. Lois, S. Lundberg, E. Moorkens, G. Motte, K.-O. Nagel, P. Ondina, A. Outeiro, M. Paunovic, V. Prié, T. von Proschwitz, N. Riccardi, M. Rudzīte, M. Rudzītis, C. Scheder, M. Seddon, H. Şereflişan, V. Simic, S. Sokolova, K. Stoeckl, J. Taskinen, A. Teixeira, F. Thielen, T. Trichkova, S. Varandas, H. Vicentini, K. Zajac, T. Zajac & S. Zogaris, 2017. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biological Reviews 92: 572–607.

    Article  Google Scholar 

  • McMahon, R. F., 1983. Ecology of an invasive pest bivalve, Corbicula. In Russell-Hunter, W. D. (ed.), The Mollusca. Academic Press, New York: 505–561.

    Google Scholar 

  • Modesto, V., M. Ilarri, A. T. Souza, M. Lopes-Lima, K. Douda, M. Clavero & R. Sousa, 2018. Fish and mussels: importance of fish for freshwater mussel conservation. Fish and Fisheries 19: 244–259.

    Article  Google Scholar 

  • Moles, K. R. & J. B. Layzer, 2008. Reproductive ecology of Actinonaias ligamentina (Bivalvia: Unionidae) in a regulated river. Journal of the North American Benthological Society 27: 212–222.

    Article  Google Scholar 

  • Mosley, T. L., W. R. Haag & J. A. Stoeckel, 2014. Egg fertilisation in a freshwater mussel: effects of distance, flow and male density. Freshwater Biology 59: 2137–2149.

    Article  Google Scholar 

  • Negishi, J. N., I. Katano & Y. Kayaba, 2011. Seasonally tracking vertical and horizontal distribution of unionid mussels (Pronodularia japanensis): implications for agricultural drainage management. Aquatic Conservation: Marine and Freshwater Ecosystems 21: 49–56.

    Article  Google Scholar 

  • Newton, T. J. & W. G. Cope, 2007. Biomarker responses of Unionid mussels to environmental contaminants. In van Hassel, J. H. & J. L. Farris (eds), Freshwater Bivalve Ecotoxicology. CRC Press, Boca Raton: 257–284.

    Google Scholar 

  • Newton, T. J., S. J. Zigler & B. R. Gray, 2015. Mortality, movement and behaviour of native mussels during a planned water-level drawdown in the Upper Mississippi River. Freshwater Biology 60: 1–15.

    Article  Google Scholar 

  • Novais, A., E. Dias & R. Sousa, 2016. Inter and intraspecific variation of carbon and nitrogen stable isotopes ratios in freshwater bivalves. Hydrobiologia 765: 149–158.

    Article  CAS  Google Scholar 

  • Páscoa, P., C. M. Gouveia, A. Russo & R. M. Trigo, 2017. Drought trends in the Iberian Peninsula over the Last 112 Years. Advances in Meteorology. https://doi.org/10.1155/2017/4653126.

    Article  Google Scholar 

  • Resgalla Jr., C., E. D. S. Brasil & L. C. Salomão, 2007. The effect of temperature and salinity on the physiological rates of the mussel Perna perna (Linnaeus 1758). Brazilian Archives of Biology and Technology 50: 543–556.

    Article  CAS  Google Scholar 

  • Santos, R. M. B., L. F. S. Fernandes, S. G. P. Varandas, M. G. Pereira, R. Sousa, A. Teixeira, M. Lopes-Lima, R. M. Cortes & F. A. L. Pacheco, 2015. Impacts of climate change and land-use scenarios on Margaritifera margaritifera, an environmental indicator and endangered species. Science of the Total Environment 511: 477–488.

    Article  CAS  Google Scholar 

  • Schwalb, A. N. & M. T. Pusch, 2007. Horizontal and vertical movements of unionid mussels in a lowland river. Journal of the North American Benthological Society 26: 261–272.

    Article  Google Scholar 

  • Sousa, R., S. Dias, L. Guilhermino & C. Antunes, 2008a. Minho River tidal freshwater wetlands: threats to faunal biodiversity. Aquatic Biology 3: 237–250.

    Article  Google Scholar 

  • Sousa, R., M. Rufino, M. Gaspar, C. Antunes & L. Guilhermino, 2008b. Abiotic impacts on spatial and temporal distribution of Corbicula fluminea (Müller, 1774) in the River Minho estuary, Portugal. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 98–110.

    Article  Google Scholar 

  • Sousa, R., A. Ferreira, F. Carvalho, M. Lopes-Lima, S. Varandas & A. Teixeira, 2018. Die-offs of the endangered pearl mussel Margaritifera margaritifera during an extreme drought. Aquatic Conservation: Marine and Freshwater Ecosystems 28: 1244–1248.

    Article  Google Scholar 

  • Trenberth, K. E., 1990. Recent observed interdecadal climate changes in the Northern Hemisphere. Bulletin of the American Meteorological Society 71: 988–993.

    Article  Google Scholar 

  • Tricarico, E., A. O. Junqueira & D. Dudgeon, 2016. Alien species in aquatic environments: a selective comparison of coastal and inland waters in tropical and temperate latitudes. Aquatic Conservation: Marine and Freshwater Ecosystems 26: 872–891.

    Article  Google Scholar 

  • Vaughn, C. C., 1997. Regional patterns of mussel species distributions in North American rivers. Ecography 20: 107–115.

    Article  Google Scholar 

  • Vaughn, C. C. & C. C. Hakenkamp, 2001. The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46: 1431–1446.

    Article  Google Scholar 

  • Vaughn, C. C. & C. M. Taylor, 1999. Impoundments and the decline of freshwater mussels: a case study of an extinction gradient. Conservation Biology 13: 912–920.

    Article  Google Scholar 

  • Verdú, J. R. & E. Galante, 2006. Libro Rojo de los Invertebrados de España. Dirección General para la Biodiversidad. Ministerio de Medio Ambiente, Madrid.

    Google Scholar 

  • Vitousek, P. M., C. M. D’Antonio, L. L. Loope, M. Rejmánek & R. Westbrooks, 1997. Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21: 1–16.

    Google Scholar 

  • Wächtler, K., M. C. Dreher-Mansur & T. Richter, 2001. Larval types and early post larval biology in naiads (Unionoida). In Bauer, G. & K. Wächtler (eds), Ecology and evolution of freshwater mussels Unionoida. Springer-Verlag, Berlin: 93–125.

    Chapter  Google Scholar 

  • Waller, D. L., J. J. Rach, W. G. Cope & G. A. Miller, 1995. Effects of handling and aerial exposure on the survival of unionid mussels. Journal of Freshwater Ecology 10: 199–207.

    Article  Google Scholar 

  • Waller, D. L., S. Gutreuter & J. J. Rach, 1999. Behavioral responses to disturbance in freshwater mussels with implications for conservation and management. Journal of the North American Benthological Society 18: 381–390.

    Article  Google Scholar 

  • Wotton, R. S. & B. Malmqvist, 2001. Feces in aquatic ecosystems. BioScience 51: 537–544.

    Article  Google Scholar 

  • Xie, Q. & G. M. Burnell, 1995. The effect of activity on the physiological rates of two clam species, Tapes philippinarum (Adams & Reeve) and Tapes decussatus (Linnaeus). Biology and Environment: Proceedings of the Royal Irish Academy 95: 217–223.

    Google Scholar 

  • Zajac, K. & T. Zajac, 2011. The role of active individual movement in habitat selection in the endangered freshwater mussel Unio crassus Philipsson, 1788. Journal of Conchology 40: 446–461.

    Google Scholar 

  • Zimmerman, G. F. & F. A. de Szalay, 2007. Influence of unionid mussels (Mollusca: Unionidae) on sediment stability: an artificial stream study. Fundamental and Applied Limnology 168: 299–306.

    Article  Google Scholar 

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Acknowledgements

I am very grateful to Laura Fandiño that actively worked monitoring the mussels and who is largely responsible for its successful outcome. I am very grateful to Prof. Isabel Pardo for its unconditional support. I greatly appreciate the Oklahoma Biological Survey, especially Prof. Caryn Vaughn, for her support on this manuscript and for providing a quiet place for work and write this manuscript in the U.S. Also, I am grateful for the inspiration provided by a large group of experts worldwide to decipher the causes responsible of mussels decline. I also wish to thank Dr. Manuel Lopes-Lima, Dr. Luigi Naselli-Flores, Dr. Ronaldo Sousa and one anonymous reviewer for comments on this manuscript. Financial support came from a pre-doctoral (Xunta de Galicia Plan I2C 2013-2016, PRE/2013/400) and a post-doctoral (Xunta de Galicia Plan I2C 2017-2020, 09.40.561B.444.0) fellowship from the government of the autonomous community of Galicia.

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Ferreira-Rodríguez, N. Spatial aggregation of native with non-native freshwater bivalves and activity depletion under summer heat waves: ‘dangerous liaisons’ in a climate change context. Hydrobiologia 834, 75–85 (2019). https://doi.org/10.1007/s10750-019-3910-2

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