Effects of thermal and hypoxic stress on respiratory patterns of three unionid species: implications for management and conservation

  • Austin Haney
  • Hisham Abdelrahman
  • James A. StoeckelEmail author
Primary Research Paper


Mussels are at particular risk from thermal stress and hypoxia due to limited range and mobility. Of interest to managers is whether sensitivity is uniform or varies among species and subpopulations. We used respirometry to investigate effects of temperature on energy demand and hypoxia tolerance of two narrowly distributed species (Cyclonaias petrina, Colorado River; C. necki, Guadalupe River), and two subpopulations of a widely distributed species (C. pustulosa: Colorado and Navasota rivers) in central Texas. We observed zero mortality during acclimation and respirometry runs even when mussels were exposed to hypoxic conditions for several hours at 36 °C. However, type and magnitude of sublethal effects varied across species and subpopulations as temperatures increased. C. pustulosa (Colorado River) exhibited the greatest increase in energy demand, C. petrina exhibited a decreasing ability to regulate oxygen consumption and an increase in critical dissolved oxygen concentration, C. pustulosa (Navasota River) exhibited metabolic depression, and both C. petrina and C. necki exhibited increasing frequency of valve closure. Results suggest that effects of increasing temperature on energetic requirements are more important than effects on hypoxia tolerance. Management strategies considering physiological differences among species and/or subpopulations are likely to be more effective than a simple “one-size-fits-all” approach.


Dissolved oxygen Respiration Energy demand Climate change Valve closure Temperature Hypoxia 



This research was supported by the Alabama Agricultural Experiment Station and the Hatch program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. Funding was provided by the Texas Comptroller of Public Accounts and Texas State University Subcontract 17,012-82683-1. We thank B. Littrell, K. Sullivan, J. Guajardo, and J. Jenkerson of BIOWEST, Inc. for mussel field collections. Lab members Ryan Fluharty, Kaelyn Fogelman, and Rebecca Gibson provided much appreciated help throughout this project.


  1. Anestis, A., A. Lazou, H. O. Pörtner & B. Michaelidis, 2007. Behavioural, metabolic and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 293: R911–R921.CrossRefGoogle Scholar
  2. ASTM, 2013. Standard Guide for Conducting Laboratory Toxicity Tests with Freshwater Mussels. ASTM International, West Conshohocken, PA.Google Scholar
  3. Bayne, B. L., 1976. Marine Mussels: Their Ecology and Physiology, Vol. 10. Cambridge University Press, New York.Google Scholar
  4. Brown, L. R., 1989. Temperature preferences and oxygen consumption of three species of sculpin (Cottus) from the Pit River drainage, California. Environmental Biology of Fishes 26: 223–236.CrossRefGoogle Scholar
  5. Burlakova, L., A. Karatayev, E. Froufe, A. Bogan & M. Lopes-Lima, 2018. A new freshwater bivalve species of the genus Cyclonaias from Texas (Unionidae: Ambleminae: Quadrulini). The Nautilus 132: 45–50.Google Scholar
  6. Burton, T., S. S. Killen, J. D. Armstrong & N. B. Metcalfe, 2011. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proceedings of the Royal Society B: Biological Sciences 278: 3465–3473.CrossRefGoogle Scholar
  7. Chen, L. Y., A. G. Heath & R. J. Neves, 2001. Comparison of oxygen consumption in freshwater mussels (Unionidae) from different habitats during declining dissolved oxygen concentration. Hydrobiologia 450: 209–214.CrossRefGoogle Scholar
  8. Crocker, C. E. & J. J. Cech Jr., 1997. Effects of hypoxia on oxygen consumption rate and swimming activity in juvenile white sturgeon, Acipenser transmontanus, in relation to temperature and life intervals. Environmental Biology of Fishes 50: 383–389.CrossRefGoogle Scholar
  9. Ferreira-Rodriguez, 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.CrossRefGoogle Scholar
  10. Ferreira-Rodríguez, N., Y. B. Akiyama, O. V. Aksenova, R. Araujo, C. M. Barnhart, Y. V. Bespalaya, A. E. Bogan, I. N. Bolotov, P. B. Budha, C. Clavijo, S. J. Clearwater, G. Darrigran, V. T. Do, K. Douda, E. Froufe, C. Gumpinger, L. Henrikson, C. L. Humphrey, N. A. Johnson, O. Klishko, M. W. Klunzinger, S. Kovitvadhi, U. Kovitvadhi, J. Lajtner, M. Lopes-Lima, E. A. Moorkens, S. Nagayama, K. O. Nagel, M. Nakano, J. N. Negishi, P. Ondina, P. Oulasvirta, V. Prié, N. Riccardi, M. Rudzīte, F. Sheldon, R. Sousa, D. L. Strayer, M. Takeuchi, J. Taskinen, A. Teixeira, J. S. Tiemann, M. Urbańska, S. Varandas, M. V. Vinarski, B. J. Wicklow, T. Zając & C. C. Vaughn, 2019. Research priorities for freshwater mussel conservation assessment. Biological Conservation 231: 77–87.CrossRefGoogle Scholar
  11. Freshwater Mollusk Conservation Society, 2016. A national strategy for the conservation of native freshwater mollusks. Freshwater Mollusk Biology and Conservation 19: 1–21.Google Scholar
  12. Gagnon, P. M., S. W. Golladay, W. K. Michener & M. C. Freeman, 2004. Drought responses of freshwater mussels (Unionidae) in coastal plain tributaries of the Flint River basin, Georgia. Journal of Freshwater Ecology 19: 667–679.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Gates, K. K., C. C. Vaughn & J. P. Julian, 2015. Developing environmental flow recommendations for freshwater mussels using the biological traits of species guilds. Freshwater Biology 60: 620–635.CrossRefGoogle Scholar
  15. Gnaiger, E., 1983a. Heat dissipation and energetic efficiency in animal anoxibiosis: economy contra power. Journal of Experimental Zoology 228: 471–490.CrossRefGoogle Scholar
  16. Gnaiger, E., 1983b. Appendix C Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In Gnaiger, E. & H. Forstner (eds), Polarographic Oxygen Sensors: Aquatic and Physiological Applications. Springer-Verlag, New York: 337–345.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Johnson, N. A., C. H. Smith, J. M. Pfeiffer, C. R. Randklev, J. D. Williams & J. D. Austin, 2018. Integrative taxonomy resolves taxonomic uncertainty for freshwater mussels being considered for protection under the US Endangered Species Act. Scientific Reports 8: 15892.CrossRefGoogle Scholar
  19. Kaushal, S. S., G. E. Likens, N. A. Jaworski, M. L. Pace, A. M. Sides, D. Seekell, D. H. Secor & R. L. Wingate, 2010. Rising stream and river temperatures in the United States. Frontiers in Ecology and the Environment 8: 461–466.CrossRefGoogle Scholar
  20. Marshall, D. J., Y. Dong, C. D. McQuaid & G. A. Williams, 2011. Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. The Journal of Experimental Biology 214: 3649–3657.CrossRefGoogle Scholar
  21. Master, L. L., B. A. Stein, L. S. Kutner & G. A. Hammerson, 2000. Vanishing assets: conservation status of U.S. species. In Stein, B. A., L. S. Kutner & J. S. Adams (eds), Precious Heritage: The Status of Biodiversity in the United States. Oxford University Press, New York: 93–118.Google Scholar
  22. Moore, R. D., D. L. Spittlehouse & A. Story, 2005. Riparian microclimate and stream temperature response to forest harvesting: a review. Journal of the American Water Resources Association 41: 813–834.CrossRefGoogle Scholar
  23. Mueller, C. A. & R. S. Seymour, 2011. The regulation index: a new method for assessing the relationship between oxygen consumption and environmental oxygen. Physiological and Biochemical Zoology 84: 522–532.CrossRefGoogle Scholar
  24. Newton, T., J. Sauer & B. Karns, 2013. Water and sediment temperatures at mussel beds in the upper Mississippi River basin. Walkerana 16: 53–62.Google Scholar
  25. Pandolfo, T. J., W. G. Cope, C. Arellano, R. B. Bringolf, M. C. Barnhart & E. Hammer, 2010. Upper thermal tolerances of early life stages of freshwater mussels. Journal of the North American Benthological Society 29: 959–969.CrossRefGoogle Scholar
  26. Payton, S. L., P. D. Johnson & M. J. Jenny, 2016. Comparative physiological, biochemical and molecular thermal stress response profiles for two unionid freshwater mussel species. Journal of Experimental Biology 219: 3562–3574.CrossRefGoogle Scholar
  27. Randklev, C. R., E. T. Tsakris, M. S. Johnson, T. Popejoy, M. A. Hart, J. Khan, D. Geeslin & C. R. Robertson, 2018. The effect of dewatering on freshwater mussel (Unionidae) community structure and the implications for conservation and water policy: a case study from a spring-fed stream in the southwestern United States. Global Ecology and Conservation 16: 1–15.CrossRefGoogle Scholar
  28. Rogers, N. J., M. A. Urbina, E. E. Reardon, D. J. McKenzie & R. W. Wilson, 2016. A new analysis of hypoxia tolerance in fishes using a database of critical oxygen level (Pcrit). Conservation Physiology 4: cow012.CrossRefGoogle Scholar
  29. Smith, M. E., J. M. Lazorchak, L. E. Herrin, S. Brewer-Swartz & W. T. Thoeny, 1997. A reformulated, reconstituted water for testing the freshwater amphipod, Hyalella azteca. Environmental Toxicology and Chemistry 16: 1229–1233.CrossRefGoogle Scholar
  30. Spooner, D. E. & C. C. Vaughn, 2008. A trait-based approach to species’ roles in stream ecosystems: climate change, community structure, and material cycling. Oecologia 158: 307–317.CrossRefGoogle Scholar
  31. Verberk, W. C., D. T. Bilton, P. Calosi & J. I. Spicer, 2011. Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns. Ecology 92: 1565–1572.CrossRefGoogle Scholar
  32. Walsh, S. J., D. C. Haney & C. M. Timmerman, 1997. Variation in thermal tolerance and routine metabolism among spring-and stream dwelling freshwater sculpins (Teleostei: Cottidae) of the southeastern United States. Ecology of Freshwater Fish 6: 84–94.CrossRefGoogle Scholar
  33. Wood, C. M., 2018. The fallacy of the Pcrit—are there more useful alternatives? Journal of Experimental Biology 221: jeb163717.CrossRefGoogle Scholar
  34. Xenopoulos, M. A., D. M. Lodge, J. Alcamo, M. Märker, K. Schulze & D. P. Van Vuuren, 2005. Scenarios of freshwater fish extinctions from climate change and water withdrawal. Global Change Biology 11: 1557–1564.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Fisheries, Aquaculture, and Aquatic SciencesAuburn UniversityAuburnUSA
  2. 2.Department of Veterinary Hygiene and Management, Faculty of Veterinary MedicineCairo UniversityGizaEgypt

Personalised recommendations