, Volume 701, Issue 1, pp 37–49 | Cite as

Juvenile Ribbontail Stingray, Taeniura lymma (Forsskål, 1775) (Chondrichthyes, Dasyatidae), demonstrate a unique suite of physiological adaptations to survive hyperthermic nursery conditions

  • Theresa F. Dabruzzi
  • Wayne A. Bennett
  • Jodie L. Rummer
  • Nann A. Fangue
Primary Research Paper


Juvenile ribbontail stingrays, Taeniura lymma (Forsskål, 1775) of the tropical West Pacific inhabit mangal and seagrass nurseries that often experience rapid and extreme increases in water temperature. We hypothesized that juvenile rays possess a thermal strategy similar to other hyperthermic specialists, in which fish prefer high temperatures, are always prepared for thermal extremes regardless of previous thermal history, and exhibit low metabolic thermal sensitivity. Critical thermal methodology was used to determine the thermal niche, and a thermal gradient used to estimate stingray final preferendum. Temperature quotients (Q 10) were calculated from metabolic rates determined at three temperatures using flow-through respirometry. As predicted, juvenile rays showed a relatively small thermal niche dominated by intrinsic tolerance with limited capacity for acclimation. Thermal preference values were higher than those reported for other elasmobranch species. Interestingly, the temperature quotient for juvenile rays was higher than expected, suggesting that these fish may have the ability to exploit the thermal heterogeneity in their environment. Temperature likely acts as a directing factor in this species, separating warm tolerant juveniles from adults living in deeper, cooler waters.


Temperature preference Q10 Metabolism Temperature tolerance polygon CTM Elasmobranch 



We thank Operation Wallacea, University of West Florida Research and Sponsored Programs, the Department of Biology, and the University of California Agricultural Experiment Station (grant no. 2098-H to N.A.F.) for providing funding. All animals in this study were treated in accordance with guidelines approved by the University of West Florida Animal Care and Use Committee (Protocol #2010-004).


  1. Angilletta, M. J. Jr., A. F. Bennett, H. Guderley, C. A. Navas, F. Seebacher & R. S. Wilson, 2006. Coadaptation: a unifying principle in evolutionary thermal biology. Physiological and Biochemical Zoology 79: 282–294.PubMedCrossRefGoogle Scholar
  2. Baldwin, C. M., D. A. Beauchamp & C. P. Gubala, 2002. Seasonal and diel distribution and movement of cutthroat trout from ultrasonic telemetry. Transactions of the American Fisheries Society 131: 143–158.CrossRefGoogle Scholar
  3. Becker, C. D. & R. G. Genoway, 1979. Evaluation of the critical thermal maximum for determining thermal tolerance of freshwater fish. Environmental Biology of Fishes 4: 245–256.CrossRefGoogle Scholar
  4. Beitinger, T. L. & R. W. McCauley, 1990. Whole-animal physiological processes for the assessment of stress in fishes. International Association for Great Lakes Research 16: 542–575.CrossRefGoogle Scholar
  5. Beitinger, T. L., W. A. Bennett & R. W. McCauley, 2000. Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environmental Biology of Fishes 58: 237–275.CrossRefGoogle Scholar
  6. Bennett, W. A., 2010. Extreme physiology of intertidal fishes of the Wakatobi. In Clifton, J., R. K. F. Unsworth & D. J. Smith (eds), Marine research and conservation in the Coral Triangle: The Wakatobi National Park. Nova Science Publishers, Hauppauge, NY.Google Scholar
  7. Bennett, W. A. & T. L. Beitinger, 1997. Temperature tolerance of the sheepshead minnow, Cyprinodon variegatus. Copeia 1997: 77–87.CrossRefGoogle Scholar
  8. Bennett, W. A., R. W. McCauley & T. L. Beitinger, 1998. Rates of gain and loss of heat tolerance in channel catfish. Transactions of the American Fisheries Society 127: 1053–1060.CrossRefGoogle Scholar
  9. Berge, H. B, 2009. Effects of a temperature-oxygen squeeze on distribution, feeding, growth, and survival of kokanee (Oncorhynchus nerka) in Lake Sammamish, Washington, Dissertation, University of Washington, Seattle.Google Scholar
  10. Carlson, J. K. & G. R. Parsons, 1999. Seasonal differences in routine oxygen consumption rates of the bonnethead shark. Journal of Fish Biology 55: 876–879.CrossRefGoogle Scholar
  11. Casterlin, M. E. & W. W. Reynolds, 1979. Shark thermoregulation. Comparative Biochemistry and Physiology 64A: 451–453.Google Scholar
  12. Cavanagh, R. D., P. M. Kyne, S. L. Fowler, J. A. Musick & M. B. Bennett (eds), 2003. The Conservation Status of Australian Chondrichthyans: Report of the IUCN Shark Specialist Group Australia and Oceania Regional Red List Workshop. University of Queensland, School of Biomedical Sciences, Brisbane.Google Scholar
  13. Cech, J. J., 1990. Respirometry. In Schreck, C. B. & P. B. Moyle (eds), Methods for Fish Biology. American Fisheries Society, Bethesda: 335–356.Google Scholar
  14. Chin, A., M. K. Peter, T. I. Walker & R. B. McAuley, 2010. An integrated risk assessment for climate change: analyzing the vulnerability of sharks and rays on Australia’s Great Barrier Reef Global Change Biology 16: 1936–1953.Google Scholar
  15. Chung, K. S., 1980. Rate of acclimation of the tropical saltmarsh fish Cyprinodon dearborni to temperature changes. Hydrobiologia 78: 177–181.CrossRefGoogle Scholar
  16. Claussen, D. L., 1977. Thermal acclimation in ambystomatid salamanders. Comparative Biochemistry and Physiology 58A: 333–340.Google Scholar
  17. Coutant, C. C., 1985. Striped bass, temperature, and dissolved oxygen: a speculative hypothesis for environmental risk. Transactions of the American Fisheries Society 114: 31–61.CrossRefGoogle Scholar
  18. Coutant, C. C., 1977. Compilation of temperature preference data. Journal of the Fisheries Research Board of Canada 34: 739–745.CrossRefGoogle Scholar
  19. Cowles, R. B. & C. M. Bogert, 1944. A preliminary study of the thermal requirements of desert reptiles. Bulletin of the American Museum of Natural History 83: 265–296.Google Scholar
  20. Cox, D. K., 1974. Effects of three heating rates on the critical thermal maximum of bluegill. In Gibbons, J. W., & R. R. Sharitz (eds), Thermal Ecology Conference No. 730505. National Technical Information Service, Springfield, VA: 158–163.Google Scholar
  21. Cox, G. W., 1990. Laboratory Manual of General Ecology, 6th ed. William C. Brown Publishers, Dubuque.Google Scholar
  22. Crawshaw, L. I. & H. T. Hammel, 1973. Behavioral temperature regulation in the California horn shark, Heterodontus francisci. Brain, Behavior and Evolution 7: 447–452.PubMedCrossRefGoogle Scholar
  23. DiGirolamo, A. L., S. H. Gruber, C. Pomory & W. A. Bennett, 2012. Diel patterns of temperature selection from juvenile lemon sharks, Negaprion brevirostris, in a shallow water nursery. Journal of Fish Biology 80: 1436–1448.Google Scholar
  24. Di Santo, V. & W. A. Bennett, 2011. Is post-feeding thermotaxis advantageous in elasmobranch fishes? Journal of Fish Biology 78: 195–207.PubMedCrossRefGoogle Scholar
  25. El-dawi, E. F. A., 2000. Diversity, habitats & seasonal distributions of fish in three protectorates of Sinai on the Red Sea. Egypt. Qatar University Science Journal 20: 111–124.Google Scholar
  26. Eme, J. & W. A. Bennett, 2009a. Acute temperature quotient responses of fishes reflect their divergent thermal habitats in the Banda Sea, Sulawesi, Indonesia. Australian Journal of Zoology 57: 357–362.CrossRefGoogle Scholar
  27. Eme, J. & W. A. Bennett, 2009b. Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. Journal of Thermal Biology 34: 220–225.CrossRefGoogle Scholar
  28. Fangue, N. A. & W. A. Bennett, 2003. Thermal tolerance responses of laboratory-acclimated and seasonally-acclimatized Atlantic stingray, Dasyatis sabina. Copeia 2003: 315–325.CrossRefGoogle Scholar
  29. Fast, A. W., 1973. Effects of artificial hypolimnion aeration on rainbow trout (Salmo gairdneri) depth distributions in a northern Michigan lake. Transactions of the American Fisheries Society 102: 715–722.CrossRefGoogle Scholar
  30. Fowler, S. L., T. M. Reed & F. A. Dipper, 1997. The IUNC Species Survival Commission, No. 25: Elasmobranch Biodiversity Conservation and Management. Proceedings of the International Seminar and Workshop, Sabah, Malaysia, July 1997.Google Scholar
  31. Fry, F. E. J, 1947. Effects of the environment on animal activity. University of Toronto Studies, Biological Series 55. Publication of the Ontario Fisheries Research Laboratory, Vol. 68: 1–62.Google Scholar
  32. Fry, F. E. J., 1971. The Effect of Environmental Factors on the Physiology of Fish. Fish physiology. Academic Press, New York.Google Scholar
  33. Garrone-Neto, D. & I. Sazima, 2009. Stirring, charging, and picking: hunting tactics of potamotrygonid rays in the upper Paraná River. Neotropical Ichthyology 7: 113–116.Google Scholar
  34. Gebhart, G. E. & R. C. Summerfelt, 1978. Seasonal growth rates of fishes in relation to conditions of lake stratification. Proceedings of the Oklahoma Academy of Sciences 58: 6–10.Google Scholar
  35. Hochachka, P. W. & G. N. Somero, 1973. Strategies of Biochemical Adaptation. W. B. Saunders Co., Philadelphia.Google Scholar
  36. Hochachka, P. W. & G. N. Somero, 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, New York.Google Scholar
  37. Hopkins, T. E. & J. J. Cech Jr, 1994. Effect of temperature on oxygen consumption of the bat ray, Myliobatis californica (Chondrichthyes, Mylobatididae). Copeia 1994: 529–532.CrossRefGoogle Scholar
  38. Huffard, C. L., 2007. Ethogram of Abdopus Aculeatus (D’orbigny, 1834) (Cephalopoda: Octopodidae): can behavioural characters inform octopodid taxomony & systematics? Journal of Molluscan Studies 73: 185–193.CrossRefGoogle Scholar
  39. IPCC, 2007. Climate change 2007: the physical science basis. In Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.Google Scholar
  40. IUCN, 2011. IUCN Red List of Threatened Species. Version 2011.2 [available on internet at].
  41. Last, P. R. & J. D. Stevens, 1994. Sharks and Rays of Australia, 2nd ed. CSIRO Publishing, Melbourne.Google Scholar
  42. Lugendo, B. R., I. Nagelkerken, N. Jiddawi, Y. D. Mgaya & G. Van Der Velde, 2007. Fish community composition of a tropical nonestuarine embayment in Zanzibar, Tanzania. Fisheries Science 73: 1213–1223.Google Scholar
  43. Lutterschmidt, W. I. & V. H. Hutchison, 1997. The critical thermal maximum: data to support the onset of muscle spasm as the definitive end point. Canadian Journal of Zoology 75: 1553–1560.CrossRefGoogle Scholar
  44. Matern, S. A., J. J. Cech Jr & T. E. Hopkins, 2000. Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation? Environmental Biology of Fishes 58: 173–182.CrossRefGoogle Scholar
  45. McCauley, R. W. & N. W. Huggins, 1979. Ontogenetic and non-thermal seasonal effects on thermal preferenda of fish. American Zoologist 19: 267–271.Google Scholar
  46. Meloni, C. J., J. J. Cech & S. M. Katzman, 2002. Effect of brackish salinities on oxygen consumption of bat rays (Myliobatis californica). Copeia 2002: 462–465.CrossRefGoogle Scholar
  47. Michael, S. W., 1993. Reef Sharks & Rays of the World: A guide to Their identification, Behavior, and Ecology. Sea Challengers, Monteray.Google Scholar
  48. Munday, P. L., G. P. Jones, M. S. Pratchett & A. J. Williams, 2008. Climate change and the future for coral reef fishes. Fish and Fisheries 9: 261–285.CrossRefGoogle Scholar
  49. Meysman, F. J. R., J. J. Middelburg & C. H. R. Hiep, 2006. Bioturbation: a fresh look at Darwin’s last idea. TRENDS in Ecology and Evolution 21: 688–695.PubMedCrossRefGoogle Scholar
  50. Neer, J. A., J. K. Carlson & B. A. Thompson, 2006. Standard oxygen consumption of seasonally acclimatized cownose rays, Rhinoptera bonasus (Mitchill 1815), in the Northern Gulf of Mexico. Fish Physiology and Biochemistry 32: 67–71.PubMedCrossRefGoogle Scholar
  51. Nestler, J. M., R. A. Goodwin, T. M. Cole, D. Degan & D. Dennerline, 2002. Simulating movement patterns of blueback herring in a stratified southern impoundment. Transactions of the American Fisheries Society 131: 55–69.CrossRefGoogle Scholar
  52. Newell, R. C. & H. R. Northcroft, 1967. A reinterpretation of the effect of temperature on the metabolism of certain marine invertebrates. Journal of Zoology 151: 277–298.Google Scholar
  53. Nguyen, N. T. & V. Q. Nguyen, 2006. Biodiversity and living resources of the coral reef fishes in Vietnam marine waters. Science and Technology Publishing House, Hanoi.Google Scholar
  54. O’Shea, O. R., M. Thums, M. van Keulen & M. Meekan, 2011. Bioturbation by stingrays at Ningaloo Reef, Western Australia. Marine and Freshwater Research 62: 1323–1650.Google Scholar
  55. Paladino, R. V., J. R. Spotila, J. P. Schubauer & K. T. Kowalski, 1980. The critical thermal maximum: a technique used to elucidate physiological stress and adaptation in fishes. Revue Canadienne de Biologie 39: 115–122.Google Scholar
  56. Perry, A. L., P. J. Low, J. R. Ellis & J. D. Reynolds, 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912–1915.PubMedCrossRefGoogle Scholar
  57. Poloczanska, E. S., R. C. Babcock, A. Butler, A. J. Hobday, O. Hoegh-Guldberg, T. J. Kunz, et al., 2007. Climate change and Australian marine life. In Gibson, R. N., J. D. M. Gordon & R. J. A. Atkinson (eds), Oceanography and Marine Biology. Taylor & Francis, New York: 407–478.Google Scholar
  58. Portner, H. O. & A. P. Farrell, 2008. Physiology and climate change. Science 322: 690–692.PubMedCrossRefGoogle Scholar
  59. Portner, H. O. & R. Knust, 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95–97.PubMedCrossRefGoogle Scholar
  60. Reber, C. S. & W. A. Bennett, 2007. The influence of thermal parameters on the acclimation responses of pinfish, Lagodon rhomboides, exposed to decreasing temperatures. The Journal of Fish Biology 71: 833–841.CrossRefGoogle Scholar
  61. Reynolds, W. W. & M. E. Casterlin, 1979. Behavioral thermoregulation and the “final preferendum” paradigm. American Zoologist 19: 211–224.Google Scholar
  62. Rowe, D. K. & B. L. Chisnall, 1995. Effects of oxygen, temperature and light gradients on the vertical distribution of rainbow trout, Oncorhynchus mykiss, in two North Island, New Zealand, lakes differing in trophic status. New Zealand Journal of Marine and Freshwater Research 29: 421–434.CrossRefGoogle Scholar
  63. Schmidt-Nielsen, K., 1997. Animal Physiology: Adaptation and environment, 5th ed. Cambridge University Press, Cambridge.Google Scholar
  64. Schulte, P. M., T. M. Healy & N. A. Fangue, 2011. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integrative and Comparative Biology 51: 691–702.PubMedCrossRefGoogle Scholar
  65. Sims, D. W., V. J. Wearmouth, E. J. Southall, J. M. Hill, P. Moore, K. Rawlinson, et al., 2006. Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. Journal of Animal Ecology 75: 176–190.PubMedCrossRefGoogle Scholar
  66. Steffensen, J. F., 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry 6: 49–59.CrossRefGoogle Scholar
  67. Stevens, E. D., 1992. Use of plastic materials in oxygen-measuring systems. Journal of Applied Physiology 72: 801–804.PubMedGoogle Scholar
  68. Sumner, F. B. & P. Doudoroff, 1938. Some experiments upon temperature acclimatization and respiratory metabolism in fishes. Biological Bulletin 74: 403–429.CrossRefGoogle Scholar
  69. Taylor, J. R., M. M. Cook, A. L. Kirkpatrick, S. N. Galleher, J. Eme & W. A. Bennett, 2005. Thermal tactics of air-breathing and non air-breathing gobiids inhabiting mangrove tidepools on Pulau Hoga, Sulawesi, Indonesia. Copeia 2005: 886–893.CrossRefGoogle Scholar
  70. Teh, L., Al S Cabanban & U. R. Sumaila, 2005. The reef fisheries of Pulau Banggi, Sabah: a preliminary profile and assessment of ecological and socio-economic sustainability. Fisheries Research 76: 359–367.CrossRefGoogle Scholar
  71. Vaudo, J. J. & C. G. Lowe, 2006. Movement patterns of the round stingray Urobatis halleri (Cooper) near a thermal outfall. Journal of Fish Biology 68: 1756–1766.CrossRefGoogle Scholar
  72. Vonk, J. A., M. J. A. Christianen & J. Stapel, 2008. Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows. Estuarine, Coastal and Shelf Science 79: 653–660.CrossRefGoogle Scholar
  73. Wallman, H. L. & W. A. Bennett, 2006. Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina. Environmental Biology of Fishes 75: 261–270.CrossRefGoogle Scholar
  74. White, W. T. & F. Dharmadi, 2007. Species and size compositions and reproductive biology of rays (Chondrichthyes, Batoidea) caught in target and non-target fisheries in eastern Indonesia. Journal of Fish Biology 70: 1809–1837.CrossRefGoogle Scholar
  75. Wilson, S. K., M. Adjeroud, D. R. Bellwood, M. L. Berumen, D. Booth, Y.-M. Bozec, P. Chabanet, et al., 2010. Crucial knowledge gaps in current understanding of climate change impacts on coral reef fishes. Journal of Experimental Biology 213: 894–900.PubMedCrossRefGoogle Scholar
  76. Zale, A. V., J. D. Wiechman, R. L. Lochmiller & J. Burroughs, 1990. Limnological conditions associated with summer mortality of striped bass in Keystone Reservoir, Oklahoma. Transactions of the American Fisheries Society 119: 72–76.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Theresa F. Dabruzzi
    • 1
  • Wayne A. Bennett
    • 1
  • Jodie L. Rummer
    • 2
  • Nann A. Fangue
    • 3
  1. 1.Department of BiologyUniversity of West FloridaPensacolaUSA
  2. 2.ARC Centre of Excellence for Coral Reef Studies, James Cook UniversityTownsvilleAustralia
  3. 3.Department of Wildlife, Fish, and Conservation BiologyUniversity of CaliforniaDavisUSA

Personalised recommendations