Fish Physiology and Biochemistry

, Volume 40, Issue 4, pp 1011–1020 | Cite as

Hypoxia effects on gill surface area and blood oxygen-carrying capacity of the Atlantic stingray, Dasyatis sabina



Atlantic stingrays, Dasyatis sabina, are common residents of shallow-water seagrass habitats that experience natural cycles of severe hypoxia during summer months. We hypothesized that stingrays exposed to hypoxic episodes would improve their hypoxia tolerance by increasing branchial surface area and altering blood oxygen-carrying capacity. To this end, we compared critical oxygen minimum, gill morphology, and hemoglobin/hematocrit levels in a control group of Atlantic stingrays held at continuous oxygen saturations of 80–90 % (≥5.5 mg/l), to treatment groups exposed to a 7-h hypoxic interval at 55 % (~4.0 mg/l), or 30 % oxygen saturation (~2.0 mg/l). Stingrays in hypoxic treatment groups significantly improved their hypoxia tolerance. Critical oxygen minimum values fell from 0.7 ± 0.11 mg/l in control fish to 0.4 ± 0.05 and 0.4 ± 0.06 mg/l in the 55 and 30 % saturation treatment groups, respectively. Mass-specific gill surface area between control fish and the 30 % saturation treatment group increased by 1.7-fold, from 85 to 142 mm2/g. Although stingrays did not show an increase in hematocrit or hemoglobin levels, production of more efficient hemoglobin isoforms could not be ruled out. An increase in hypoxia tolerance allows Atlantic stingrays to forage for longer times and across a wide range of hypoxic habitats that are less accessible to predators and competitors.


Gill remodeling Oxygen Elasmobranch Hemoglobin Hematocrit 



This project was supported by a grant from the University of West Florida Office of Research and Sponsored Programs. All animals were collected and maintained according to guidelines established by the Institutional Animal Care and Use Committee at the University of West Florida, protocol # 2009-002. The authors would like to thank David Kracov Creations for funding and inspiration.


  1. Allen TB (1999) The shark almanac. The Lyons Press, New YorkGoogle Scholar
  2. Beitinger TL, McCauley RW (1990) Whole-animal physiological processes for the assessment of stress in fishes. J Great Lakes Res 16:542–575CrossRefGoogle Scholar
  3. Bennett WA, Beitinger TL (1995) Technical notes: overview of techniques for removing oxygen from water and a description of a new oxygen depletion system. Prog Fish Cult 57:84–87CrossRefGoogle Scholar
  4. Brill R, Bushnell P, Schroff S, Seifert R, Galvin M (2008) Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of sandbar shark (Carcharhinus plumbeus). J Exp Mar Biol Ecol 354:132–143CrossRefGoogle Scholar
  5. Cain DK, Harms CA, Segars A (2004) Plasma biochemistry reference values of wild-caught southern stingrays (Dasyatis americana). J Zoo Wildl Med 35:471–476PubMedCrossRefGoogle Scholar
  6. Cameron JN, Randall DJ, Davis JC (1971) Regulation of the ventilation-perfusion ratio in the gills of Dasyatis sabina and Squalus suckleyi. Comp Biochem Physiol A: Mol Integr Physiol 39:505–519CrossRefGoogle Scholar
  7. Carlson JK, Parsons GR (2003) Respiratory and hematological responses of the bonnethead shark, Sphyrna tiburo, to acute changes in dissolved oxygen. J Exp Mar Biol Ecol 294:15–26CrossRefGoogle Scholar
  8. Chabot D, Claireaux G (2008) Environmental hypoxia as a metabolic constraint on fish: the case of Atlantic cod, Gadus morhua. Mar Pollut Bull 57:287–294PubMedCrossRefGoogle Scholar
  9. Chapman LG, Galis F, Shinn J (2000) Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid. Ecol Lett 3:387–393CrossRefGoogle Scholar
  10. Cook DA (1994) Temporal patterns of food habits of the Atlantic stingray, Dasyatis sabina (Lesueur, 1824) from the Banana River Lagoon Florida. Master’s thesis, Florida Institute of TechnologyGoogle Scholar
  11. Craig PM, Wood CM, McClelland GB (2007) Gill membrane remodeling with soft-water acclimation in zebrafish (Danio rerio). Physiol Genom 30:53–60CrossRefGoogle Scholar
  12. Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78:195–207PubMedCrossRefGoogle Scholar
  13. Fangue NA, Bennett WA (2003) Thermal tolerance responses of laboratory-acclimated and seasonally acclimatized Atlantic stingray, Dasyatis sabina. Copeia 2003:315–325CrossRefGoogle Scholar
  14. Farrell AP (1993) Cardiovascular system. In: Evans DH (ed) The physiology of Fishes. CRC Press, Boca RatonGoogle Scholar
  15. Ferer EJ (2007) Salinity effect on urea and TMAO levels in blood plasma of Atlantic stingray, Dasyatis Sabina. Master’s thesis. University of West FloridaGoogle Scholar
  16. Filho DW, Eble GJ, Kassner G, Caprario FX, Dafré AL, Ohira M (1992) Comparative hematology in marine fish. Comp Biochem Physiol A Physiol 102:311–321CrossRefGoogle Scholar
  17. Filho DW, Torres MA, Zaniboni-Filho E, Pedrosa RC (2005) Effect of different oxygen tension on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes, 1847). Aqua 244:349–357CrossRefGoogle Scholar
  18. Friedman JR, Condon NE, Drazen JC (2012) Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California. Limnol Oceanogr 57:1701–1710CrossRefGoogle Scholar
  19. Fu SJ, Brauner CJ, Cao ZD, Richards JG, Peng JL, Dhillon R, Wang YX (2011) The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). J Exp Biol 214:2080–2088PubMedCrossRefGoogle Scholar
  20. Gilbert CR, Williams JD (2002) National Audubon Society field guide to fishes. Alfred Knopf, New YorkGoogle Scholar
  21. Gonzalez RJ, McDonald DG (1992) The relationship between oxygen consumption and ion loss in a freshwater fish. J Exp Biol 163:317–332Google Scholar
  22. Grim JM, Ding AA, Bennett WA (2012) Differences in activity level between cownose rays (Rhinoptera bonasus) and Atlantic stingrays (Dasyatis sabina) are related to differences in heart mass, hemoglobin concentration, and gill surface area. Fish Physiol Biochem 38:1409–1417PubMedCrossRefGoogle Scholar
  23. Gudger EW (1946) Does the stingray strike and poison fishes? Sci Mon 63:110–116PubMedGoogle Scholar
  24. Gunter G (1967) Vertebrates in hypersaline waters. Contr Mar Sci 12:230–241Google Scholar
  25. Hall FG, Gray IE (1929) The hemoglobin concentration of the blood of marine fishes. J Biol Chem 81:589–594Google Scholar
  26. Holeton GF, Randall DJ (1967) Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46:297–305PubMedGoogle Scholar
  27. Huang CY, Lin HC (2011) The effect of acidity on gill variations in the aquatic airbreathing fish, Trichogaster lalius. Comp Biochem Physiol A: Mol Integr Physiol 158:61–67CrossRefGoogle Scholar
  28. Hughes GM (1984) Measurement of gill area in fishes: practices and problems. J Exp Mar Biol Ass UK 64:637–655CrossRefGoogle Scholar
  29. Johnson MR, Snelson FF Jr (1996) Reproductive life history of the Atlantic Stingray, Dasyatis sabina (Pisces: Dasyatidae), in the freshwater St. Johns River, Florida. Bull Mar Sci 59:74–88Google Scholar
  30. Kajiura S, Tricas T (1996) Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina. J Exp Biol 199:2297–2306PubMedGoogle Scholar
  31. Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc 276:735–744CrossRefGoogle Scholar
  32. McLeod TF, Sigel MM, Yunis AA (1978) Regulation of erythropoiesis in the Florida gar Lepisosteus platyrhincus. Comp Biochem Physiol A Physiol 60:145–150CrossRefGoogle Scholar
  33. Mueller ME, Sanchez DA, Bergman HL, McDonald DG, Rhem RG, Wood CM (1991) Gill Histology II. Nature and time course of acclimation to aluminium in juvenile brook trout (Salvelinus fontinalis). Can J Fish Aqua Sci 48:2016–2027CrossRefGoogle Scholar
  34. Muir BS, Hughes GM (1969) Gill dimensions for three species of tunny. J Exp Biol 51:271–285Google Scholar
  35. Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090PubMedCrossRefGoogle Scholar
  36. Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409PubMedCrossRefGoogle Scholar
  37. Nilsson GE, Östlund-Nilsson S (2008) Does size matter for hypoxia tolerance in fish? Biol Rev 83:173–189PubMedCrossRefGoogle Scholar
  38. Nilsson GE, Dymowska A, Stecyk JAW (2012) New insights into the plasticity of gill structure. Respir Physiol Neuro 184:214–222CrossRefGoogle Scholar
  39. Ong KJ, Stevens ED, Wright PA (2007) Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. J Exp Biol 210:1109–1115PubMedCrossRefGoogle Scholar
  40. Perez-Dominguez R, Holt SA, Holt G (2006) Environmental variability in seagrass meadows: effects of nursery environment cycles on growth and survival in larval red drum Sciaenops ocellatus. Mar Ecol Prog 321:41–53CrossRefGoogle Scholar
  41. Perry SF, McDonald DG (1993) Gas exchange. In: Evans DH (ed) The physiology of Fishes. CRC Press, Boca RatonGoogle Scholar
  42. Perry SF, Jonz MG, Gilmour KM (2009) Chapter 5: oxygen sensing and the hypoxic ventilatory response. Fish Physiol 27:193–253CrossRefGoogle Scholar
  43. Powers DA, Dalessio PM, Lee E, DiMichele L (1986) The molecular ecology of Fundulus heteroclitus hemoglobin-oxygen affinity. Am Zool 26:235–248Google Scholar
  44. Prosser CL (1991) Comparative animal physiology. Wiley-Liss, DanversGoogle Scholar
  45. Rahman MS, Thomas P (2007) Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1α and HIF-2α, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene 396:273–282PubMedCrossRefGoogle Scholar
  46. Randall JE (1967) Food habitats of reef fishes of the West Indies. Stud Trop Ocean Miami 5:665–847Google Scholar
  47. Randall D (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100:275–288Google Scholar
  48. Routley MH, Nilsson GE, Renshaw G (2002) Exposure to hypoxia primes the respiratory and metabolic responses of the epaulette shark to progressive hypoxia. Comp Biochem Physiol A Physiol 131:313–321CrossRefGoogle Scholar
  49. Rytkönen KT, Vuori KA, Primmer CR, Nikinmaa M (2007) Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comp Biochem Physiol, Part D: Genomics Proteomics 2:177–186Google Scholar
  50. Saroglia M, Cecchini S, Terova G, Caputo A, De Stradis A (2000) Influence of environmental temperature and water oxygen concentration on gas diffusion distance in Sea bass (Dicentrarchus labrax, L.). Fish Physiol Biochem 23:55–58CrossRefGoogle Scholar
  51. Saroglia M, Terova G, Stradis A, Caputo A (2002) Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J Fish Biol 60:1423–1430CrossRefGoogle Scholar
  52. Saroglia M, Caricato G, Frittella F, Brambilla F, Terova G (2010) Dissolved oxygen regimen (PO2) may affect osmorespiratory compromise in European sea bass (Dicentrarchus labrax, L.). Ital J Anim Sci 9:e15CrossRefGoogle Scholar
  53. Schjolden J, Sørensen J, Nilsson GE, Poléo ABS (2007) The toxicity of copper to crucian carp (Carassius carassius) in soft water. Sci Total Environ 384:239–251PubMedCrossRefGoogle Scholar
  54. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, CambridgeGoogle Scholar
  55. Schwartz FJ, Dahlberg MD (1978) Biology and ecology of the Atlantic stingray, Dasyatis sabina (Pisces: Dasyatidae), in North Carolina and Georgia. NE Gulf Sci 2:1–23Google Scholar
  56. Semeniuk CA, Bourgeon S, Smith SL, Rothley KD (2009) Hematological differences between stingrays at tourist and non-visited sites suggest physiological costs of wildlife tourism. Biol Conserv 142:1818–1829CrossRefGoogle Scholar
  57. Smale MA, Rabeni CF (1995) Hypoxia and hyperthermia tolerances of headwater stream fishes. Trans Am Fish Soc 124:698–710CrossRefGoogle Scholar
  58. Snelson FF Jr, Williams-Hooper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988:729–739CrossRefGoogle Scholar
  59. Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251PubMedCrossRefGoogle Scholar
  60. Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673PubMedCrossRefGoogle Scholar
  61. Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109–1111PubMedCrossRefGoogle Scholar
  62. Sulikowski JA, Maginniss LA (2001) Effects of environmental dilution on body fluid regulation in the yellow stingray, Urolophus jamaicensis. Comp Biochem Physiol A: Mol Integr Physiol 128:223–232CrossRefGoogle Scholar
  63. Sulikowski JA, Trebergb JR, Howell WH (2003) Fluid regulation and physiological adjustments in the winter skate, Leucoraja ocellata, following exposure to reduced environmental salinities. Environ Biol Fish 66:339–348CrossRefGoogle Scholar
  64. Suzuki N, Takagi T, Sasayama Y, Kambegawa A (1995) Effects of ultimobranchialectomy on the mineral balances of the plasma and bile in the stingray (Elasmobranchii). Zoo Sci 12:239–242CrossRefGoogle Scholar
  65. Terova G, Rimoldi S, Corà S, Bernardini G, Gornati R, Saroglia M (2008) Acute and chronic hypoxia affects HIF-1α mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279:150–159CrossRefGoogle Scholar
  66. Thrasher RA (2002) Physiological, behavioral and morphological changes in bluegill and western mosquito fish exposed to moderate and marked hypoxia. Master’s thesis. University of West FloridaGoogle Scholar
  67. Tunnell JW Jr, Judd FW (2002) The Laguna Madre of Texas and Tamaulipas, 1st edn. Texas A&M University Press, College StationGoogle Scholar
  68. Tuurala H, Egginton S, Soivio A (1998) Cold exposure increases branchial water–blood barrier thickness in the eel. J Fish Biol 53:451–455Google Scholar
  69. Verde C, De Rosa MC, Giordano D, Mosca D, De Pascale D, Raiola L, Cocca E, Carratore V, Giardina B, Di Prisco G (2005) Structure, function and molecular adaptations of haemoglobins of the polar cartilaginous fish Bathyraja eatonii and Raja hyperborean. Biochem J 389:297–306PubMedCentralPubMedCrossRefGoogle Scholar
  70. Wallman HL, Bennett WA (2006) Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina. Environ Biol Fish 75:261–270CrossRefGoogle Scholar
  71. Weber RE (1982) Intraspecific adaptation of hemoglobin function in fish to oxygen availability. In: Addink ADF, Spronk N (eds) Exogenous and endogenous influences on metabolic and neural control. Pergamon Press, OxfordGoogle Scholar
  72. Weber RE, Wells RM, Rossetti JE (1983) Allosteric interactions governing oxygen equilibria in the haemoglobin system of the spiny dogfish, Squalus acanthias. J Exp Biol 103:109–120PubMedGoogle Scholar
  73. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, PhiladelphiaGoogle Scholar
  74. Wood CM, Randall DJ (1973) The influence of swimming activity on water balance in the rainbow trout (Salmo gairdneri). Comp Biochem Physiol A: Mol Integr Physiol 82:257–276Google Scholar
  75. Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Wildlife, Fish and Conservation BiologyUniversity of CaliforniaDavisUSA
  2. 2.Department of BiologyUniversity of West FloridaPensacolaUSA

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