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Freshwater acidification: an example of an endangered crayfish species sensitive to pH

Abstract

Carbon dioxide released in the atmosphere and dissolved in water leads to acidification. Relatively few studies have focused on fresh waters, where biocalcifying species are more readily impacted by changes in pH. Sensitivity to pH of an endangered calcium-demanding organism, the crayfish Austropotamobius pallipes, was investigated in the Pinail nature reserve, a natural system with 3000 permanent ponds, some inhabited by the crayfish and others not, originally due to human introduction. From the 14 chemical parameters measured in this study, the main limiting factor preventing crayfish establishment appears to be water acidity (pH < 6.8), which affects calcification, molting, growth and reproduction. We predict that 20% of the Pinail populations will disappear by 2060 due to freshwater acidification with the present level of fossil fuel consumption. Ongoing and future restoration projects for conservation of this heritage crustacean must select hard water with the highest water pH (> 7).

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References

  • Appelberg, M., 1985. Changes in haemolymph ion concentrations of Astacus astacus L. and Pacifastacus leniusculus (Dana) after exposure to low pH and aluminium. Hydrobiologia 121: 19–25.

    Article  CAS  Google Scholar 

  • Beaune, D., Y. Sellier, E. Lambert & F. Grandjean, 2017. The use of Chara spp. (Charales: Characeae) as a bioindicator of physico-chemical habitat suitability for an endangered crayfish Austropotamobius pallipes in lentic waters. Aquatic Conservation: Marine and Freshwater Ecosystems. https://doi.org/10.1002/aqc.2847.

    Google Scholar 

  • Bechmann, R. K., I. C. Taban, S. Westerlund, B. F. Godal, M. Arnberg, S. Vingen, A. Ingvarsdottir & T. Baussant, 2011. Effects of ocean acidification on early life stages of shrimp (Pandalus borealis) and mussel (Mytilus edulis). Journal of Toxicology and Environmental Health Part A 74: 424–438.

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka, M. A., 1984. Calcification in aquatic plants. Plant, Cell & Environment 7: 457–466.

    Article  CAS  Google Scholar 

  • Cairns, A. & N. Yan, 2009. A review of the influence of low ambient calcium concentrations on freshwater daphniids, gammarids, and crayfish. Environmental Reviews 17: 67–79.

    Article  CAS  Google Scholar 

  • Caldeira, K. & M. E. Wickett, 2003. Anthropogenic carbon and ocean pH. Nature 425: 365-365.

    Article  Google Scholar 

  • Caldwell, G. S., S. Fitzer, C. S. Gillespie, G. Pickavance, E. Turnbull & M. G. Bentley, 2011. Ocean acidification takes sperm back in time. Invertebrate Reproduction & Development 55: 217–221.

    Article  Google Scholar 

  • Carpenter, S. R., S. G. Fisher, N. B. Grimm & J. F. Kitchell, 1992. Global change and freshwater ecosystems. Annual Review of Ecology and Systematics 23: 119–139.

    Article  Google Scholar 

  • Chen, S. M. & J. C. Chen, 2003. Effects of pH on survival, growth, molting and feeding of giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 218: 613–623.

    Article  Google Scholar 

  • Cottin, D., D. Roussel, N. Foucreau, F. Hervant & C. Piscart, 2012. Disentangling the effects of local and regional factors on the thermal tolerance of freshwater crustaceans. Naturwissenschaften 99: 259–264.

    Article  CAS  PubMed  Google Scholar 

  • Creed, R. P, Jr. 1994. Direct and indirect effects of crayfish grazing in a stream community. Ecology 75: 2091–2103.

    Article  Google Scholar 

  • DiStefano, R. J., R. J. Neves, L. A. Heldrich & M. C. Lewis, 1991. Response of the crayfish Cambarus bartonii bartonii to acid exposure in southern Appalachian streams. Canadian Journal of Zoology 69: 1585–1591.

    Article  CAS  Google Scholar 

  • Doney, S. C., V. F. Fabry, R. A. Feely & J. A. Kleypas, 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1: 169–192.

    Article  PubMed  Google Scholar 

  • Fabry, V. J., B. A. Seibel, R. A. Feely & J. Orr, 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. Journal of Marine Science 65: 414–432.

    CAS  Google Scholar 

  • Favaro, L., T. Tirelli & D. Pessani, 2010. The role of water chemistry in the distribution of Austropotamobius pallipes (Crustacea Decapoda Astacidae) in Piedmont (Italy). Comptes Rendus Biologies 333: 68–75.

    Article  CAS  PubMed  Google Scholar 

  • Foster, J., 1995. Factors influencing the distribution and abundance of the crayfish Austropotamobius pallipes (Lereboullet) in Wales and the Marches, UK. Freshwater Crayfish 8: 78–98.

    Google Scholar 

  • France, R. L., 1984. Comparative tolerance to low pH of three life stages of the crayfish Orconectes virilis. Revue Canadienne de Zoologie 62: 2360–2363.

    Article  Google Scholar 

  • France, R. L., 1987. Calcium and trace metal composition of crayfish (Orconectes virilis) in relation to experimental lake acidification. Canadian Journal of Fisheries and Aquatic Science 44: 107–113.

    Article  CAS  Google Scholar 

  • France, R. L., 1993. Influence of lake pH on the distribution, abundance and health of crayfish in Canadian Shield lakes. Hydrobiologia 271: 65–70.

    Article  CAS  Google Scholar 

  • France, R. L. & N. C. Collins, 1993. Extirpation of crayfish in a lake affected by long-range anthropogenic acidification. Conservation Biology 7: 184–188.

    Article  Google Scholar 

  • Füreder, L., F. Gherardi, D. Holdich, J. Reynolds, P. Sibley & C. Souty-Grosset, 2010. Austropotamobius pallipes. The IUCN Red List of Threatened Species 2015-4. Endangered A2ce ver 3.1. http://www.iucnredlist.org/details/2430/0.

  • Grandjean, F., B. Cornuault, S. Archambault, M. Bramard & G. Otrebsky, 2000. Life history and population biology of the white-clawed crayfish, Austropotamobius pallipes pallipes, in a brook from the Poitou-Charentes region (France). Bulletin Français de la Pêche et de la Pisciculture 356: 55–70.

    Article  Google Scholar 

  • Greenaway, P., 1985. Calcium balance and molting in the Crustacea. Biological Reviews 60: 425–454.

    Article  CAS  Google Scholar 

  • Haddaway, N. R., R. J. G. Mortimer, M. Christmas & A. M. Dunn, 2013. Effect of pH on growth and survival in the freshwater crayfish Austropotamobius pallipes. Freshwater Crayfish 19: 53–62.

    Article  Google Scholar 

  • Haddaway, N. R., R. J. G. Mortimer, M. Christmas & A. M. Dunn, 2015. Water chemistry and endangered white-clawed Crayfish: a literature review and field study of water chemistry association in Austropotamobius pallipes. Knowledge and Management of Aquatic Ecosystems 416: 01.

    Article  Google Scholar 

  • Hammond, K. S., J. W. Hollows, C. R. Townsend & P. M. Lokman, 2006. Effects of temperature and water calcium concentration on growth, survival and moulting of freshwater crayfish, Paranephrops zealandicus. Aquaculture 251: 271–279.

    Article  CAS  Google Scholar 

  • Hasler, C. T., D. Butman, J. D. Jeffrey & C. D. Suski. 2016. Freshwater biota and rising pCO2? Ecology Letters, 19: 98–108.

    Article  PubMed  Google Scholar 

  • Hasler, C. T., J. D. Jeffrey, E. V. Schneider, K. D. Hannan, J. A. Tix & C. D. Suski. 2018. Biological consequences of weak acidification caused by elevated carbon dioxide in freshwater ecosystems. Hydrobiologia, 806: 1–12.

    Article  CAS  Google Scholar 

  • Heino, J., R. Virkkala & H. Toivonen, 2009. Climate change and freshwater biodiversity: detected patterns, future trends and adaptations in northern regions. Biological Reviews 84: 39–54.

    Article  PubMed  Google Scholar 

  • Hessen, D., G. Kristiansen & I. Lid, 1991. Calcium uptake from food and water in the crayfish Astacus astacus (L., 1758), measured by radioactive 45Ca (Decapoda, Astacidea). Crustaceana 60: 76–83.

    Article  Google Scholar 

  • Ivanina A. V., G. H. Dickinson, O. B. Matoo, R. Bagwe, A. Dickinson, E. Beniash & I. M. Sokolova. 2013. Interactive effects of elevated temperature and CO2 levels on energy metabolism and biomineralization of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Comparative Biochemistry and Physiology Part A: Molecular Integrative Physiology, 166: 101–111.

    Article  CAS  Google Scholar 

  • Jay, D. & D. M. Holdich, 1977. The pH tolerance of the crayfish Austropotamobius pallipes (Lereboullet). Freshwater Crayfish 3: 363–370.

    Google Scholar 

  • Jay, D. & D. M. Holdich, 1981. The distribution of the crayfish, Austropotamobius pallipes, in British waters. Freshwater Biology 11: 121–129.

    Article  Google Scholar 

  • Kozák, P., L. Füreder, A. Kouba, J. Reynolds & C. Souty-Grosset, 2011. Current conservation strategies for European crayfish. Knowledge and Management of Aquatic Ecosystems 401: 01.

    Article  Google Scholar 

  • Kroeker, K. J., R. L. Kordas, R. N. Crim & G. G. Singh, 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13: 1419–1434.

    Article  PubMed  Google Scholar 

  • Kroeker, K. J., R. L. Kordas, R. N. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte & J. P. Gattuso, 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krumbein, W. E., 1979. Calcification by bacteria and algae. In Trudinger, P. A. & D. J. Swaine (eds), Biogeochemical cycling of Mineral-Forming Elements. Elsevier, Amsterdam: 47–68.

    Chapter  Google Scholar 

  • Kunkel, J. G., 2013. Modeling the calcium and phosphate mineralization of American lobster cuticle 1. Canadian Journal of Fisheries and Aquatic Sciences 70: 1601–1611.

    Article  CAS  Google Scholar 

  • Long, W. C., K. M. Swiney, C. Harris, H. N. Page & R. J. Foy, 2013. Effects of ocean acidification on juvenile red king crab (Paralithodes camtschaticus) and tanner crab (Chionoecetes bairdi) growth, condition, calcification, and survival. PloS ONE 8: e60959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowenstam, H. A. & S. Weiner, 1989. On Biomineralization. Oxford University Press, New York.

    Google Scholar 

  • Lowery, R. S., 1988. Growth, moulting and reproduction. In Holdich, D. M. & R. S. Lowery (eds), Freshwater Crayfish: Biology, Management and Exploitation. Croom Helm (Chapman & Hall), London: 83–113.

    Google Scholar 

  • Luquet, G., 2012. Biomineralizations: insights and prospects from crustaceans. Zookeys 176: 103–121.

    Article  Google Scholar 

  • Malley, D. F., 1980. Decreased survival and calcium uptake by the crayfish Orconectes virilis in low pH. Canadian Journal of Fisheries and Aquatic Sciences 37: 364–372.

    Article  CAS  Google Scholar 

  • Mauro, N. A. & G. W. Moore, 1987. Effects of environmental pH on ammonia excretion, blood pH, and oxygen uptake in fresh water crustaceans. Comparative Biochemistry and Physiology 87C: 1–3.

    CAS  Google Scholar 

  • Morgan, D. O. & B. R. McMahon, 1982. Acid tolerance and effects of sublethal acid exposure on iono-regulation and acid-base status in two crayfish Procambarus clarki and Orconectes rusticus. Journal of Experimental Biology 97: 241–252.

    CAS  Google Scholar 

  • Økland, K. A. & J. Økland, 1985. Factor interaction influencing the distribution of the freshwater “shrimp” Gammarus. Oecologia 66: 364–367.

    Article  PubMed  Google Scholar 

  • Orr, J. C., V. F. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida & F. Joos, 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, J. C., G. A. McKinley, V. Bennington, H. A. Bootsma, D. J. Pilcher, R. W. Sterner & N. R. Urban. 2015. The potential for CO2-induced acidification in freshwater: A Great Lakes case study. Oceanography, 28: 136–145.

    Article  Google Scholar 

  • Préau, C., P. Dubech, Y. Sellier, M. Cheylan, F. Castelnau & D. Beaune, 2017. Amphibian Response to the Non-Native Fish, Lepomis gibbosus: The Case of the Pinail Nature Reserve, France. Herpetological Conservation and Biology 12: 616–623.

    Google Scholar 

  • R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. The R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Renberg, I., T. Korsman & N. J. Anderson, 1993. A temporal perspective of lake acidification in Sweden. Ambio 22: 264–271.

    Google Scholar 

  • Reynolds, J. D., 2002. Growth and reproduction. In Holdich, D. M. (ed.), Biology of freshwater crayfish. Blackwell Science, New York: 152–191.

    Google Scholar 

  • Reynolds, J., C. Souty-Grosset & A. Richardson, 2013. Ecological roles of crayfish in freshwater and terrestrial habitats. Freshwater Crayfish 19: 197–218.

    Google Scholar 

  • Riebesell, U., I. Zondervan, B. Rost, P. D. Tortell, R. E. Zeebe & F. M. Morel, 2000. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407: 364–367.

    Article  CAS  PubMed  Google Scholar 

  • Roer, R. & R. Dillaman, 1984. The structure and calcification of the crustacean cuticle. American Zoologist 24: 893–909.

    Article  CAS  Google Scholar 

  • Rukke, N. A., 2002. Effects of low calcium concentrations on two common freshwater crustaceans, Gammarus lacustris and Astacus astacus. Functional Ecology 16: 357–366.

    Article  Google Scholar 

  • Scalici, M. & G. Gibertini, 2009. Molt and gastroliths in Austropotamobius pallipes (Lereboullet, 1858). Knowledge and Management of Aquatic Ecosystems 14: 394–395.

    Google Scholar 

  • Schindler, D. W., 1988. Effects of acid rain on freshwater ecosystems. Science 239: 149–157.

    Article  CAS  PubMed  Google Scholar 

  • Stumm, W. & J. J. Morgan, 2012. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. Wiley, New York.

    Google Scholar 

  • Taugbøl, T., S. B. Wærvågen, A. N. Linløkken & J. Skurdal, 1997. Post-molt exoskeleton mineralization in adult noble crayfish, Astacus astacus, in three lakes with different calcium levels. Freshwater Crayfish 11: 219–226.

    Google Scholar 

  • Taylor, E. W. & N. M. Whiteley, 1989. Oxygen transport and acid-base balance in the haemolymph of the lobster, Homarus gammarus, during aerial exposure and resubmersion. Journal of Experimental Biology 144: 417–436.

    Google Scholar 

  • Travis, D. F., 1960. The deposition of the skeletal structures in the Crustacea. I. The histology of the gastrolith skeletal tissue complex and the gastrolith in the crayfish, Orconectes (Cambarus) virilis Hagen – Decapoda. Biological Bulletin 118: 137–149.

    Article  Google Scholar 

  • Trouilhé, M. C., C. Souty-Grosset, F. Grandjean & B. Parinet, 2007. Physical and chemical water requirements of the white-clawed crayfish (Austropotamobius pallipes) in western France. Aquatic Conservation: Marine and Freshwater Ecosystems 17: 520–538.

    Article  Google Scholar 

  • Turley, C., J. Blackford, S. Widdicombe, D. Lowe, P. D. Nightingale & A. P. Rees, 2006. Reviewing the impact of increased atmospheric CO2 on oceanic pH and the marine ecosystem. Avoiding Dangerous Climate Change 8: 65–70.

    Google Scholar 

  • U.I.C.N. MNHN, 2014. La Liste rouge des espèces menacées en France – Chapitre: Crustacés d’eau douce de France métropolitaine. Paris, France.

  • Whiteley, N. M., 2011. Physiological and ecological responses of crustaceans to ocean acidification. Marine Ecology Progress Series 430: 257–271.

    Article  CAS  Google Scholar 

  • Whiteley, N. M. & E. W. Taylor, 1992. Oxygen and acid-base disturbances in the hemolymph of the lobster Homarus gammarus during commercial transport and storage. Journal of Crustacean Biology 12: 19–30.

    Article  Google Scholar 

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Acknowledgements

We are grateful to the DREAL (Directions Régionales de l’Environnement, de l’Aménagement et du Logement) Nouvelle-Aquitaine, the Communauté d’Agglomération de Grand Châtellerault, the Syndicat de rivière Vienne et Affluents (SyRVA) and the Agence de l’Eau Loire-Bretagne for financial contributions. We thank A. Zylinsky, D. Jeune, P. Dubech, B. Menard, B. Parinet for field contributions and anonymous reviewers for valuable suggestions. We are also indebted to Pr. Julian Reynolds, from Trinity College of Dublin (Ireland), for improving the English of the manuscript.

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Correspondence to David Beaune.

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Beaune, D., Sellier, Y., Luquet, G. et al. Freshwater acidification: an example of an endangered crayfish species sensitive to pH. Hydrobiologia 813, 41–50 (2018). https://doi.org/10.1007/s10750-018-3504-4

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Keywords

  • Global change
  • Acidification
  • Austropotamobius pallipes
  • Decapoda
  • Freshwater
  • Biomineralization
  • Calcification
  • Molting
  • Ponds