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).
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
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.
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.
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.
Borowitzka, M. A., 1984. Calcification in aquatic plants. Plant, Cell & Environment 7: 457–466.
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.
Caldeira, K. & M. E. Wickett, 2003. Anthropogenic carbon and ocean pH. Nature 425: 365-365.
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.
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.
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.
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.
Creed, R. P, Jr. 1994. Direct and indirect effects of crayfish grazing in a stream community. Ecology 75: 2091–2103.
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.
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.
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.
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.
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.
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.
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.
France, R. L., 1993. Influence of lake pH on the distribution, abundance and health of crayfish in Canadian Shield lakes. Hydrobiologia 271: 65–70.
France, R. L. & N. C. Collins, 1993. Extirpation of crayfish in a lake affected by long-range anthropogenic acidification. Conservation Biology 7: 184–188.
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.
Greenaway, P., 1985. Calcium balance and molting in the Crustacea. Biological Reviews 60: 425–454.
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.
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.
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.
Hasler, C. T., D. Butman, J. D. Jeffrey & C. D. Suski. 2016. Freshwater biota and rising pCO2? Ecology Letters, 19: 98–108.
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.
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.
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.
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.
Jay, D. & D. M. Holdich, 1977. The pH tolerance of the crayfish Austropotamobius pallipes (Lereboullet). Freshwater Crayfish 3: 363–370.
Jay, D. & D. M. Holdich, 1981. The distribution of the crayfish, Austropotamobius pallipes, in British waters. Freshwater Biology 11: 121–129.
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.
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.
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.
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.
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.
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.
Lowenstam, H. A. & S. Weiner, 1989. On Biomineralization. Oxford University Press, New York.
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.
Luquet, G., 2012. Biomineralizations: insights and prospects from crustaceans. Zookeys 176: 103–121.
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.
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.
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.
Økland, K. A. & J. Økland, 1985. Factor interaction influencing the distribution of the freshwater “shrimp” Gammarus. Oecologia 66: 364–367.
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.
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.
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.
R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. The R Foundation for Statistical Computing, Vienna.
Renberg, I., T. Korsman & N. J. Anderson, 1993. A temporal perspective of lake acidification in Sweden. Ambio 22: 264–271.
Reynolds, J. D., 2002. Growth and reproduction. In Holdich, D. M. (ed.), Biology of freshwater crayfish. Blackwell Science, New York: 152–191.
Reynolds, J., C. Souty-Grosset & A. Richardson, 2013. Ecological roles of crayfish in freshwater and terrestrial habitats. Freshwater Crayfish 19: 197–218.
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.
Roer, R. & R. Dillaman, 1984. The structure and calcification of the crustacean cuticle. American Zoologist 24: 893–909.
Rukke, N. A., 2002. Effects of low calcium concentrations on two common freshwater crustaceans, Gammarus lacustris and Astacus astacus. Functional Ecology 16: 357–366.
Scalici, M. & G. Gibertini, 2009. Molt and gastroliths in Austropotamobius pallipes (Lereboullet, 1858). Knowledge and Management of Aquatic Ecosystems 14: 394–395.
Schindler, D. W., 1988. Effects of acid rain on freshwater ecosystems. Science 239: 149–157.
Stumm, W. & J. J. Morgan, 2012. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. Wiley, New York.
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.
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.
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.
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.
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.
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.
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.
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.
Handling editor: Lee B. Kats
Rights and permissions
About this article
Cite this article
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
- Global change
- Austropotamobius pallipes