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

Fish Physiology and Biochemistry

Volumn 40, Issue 4, 2014, Pages 1011-1020

  Dabruzzi, Theresa F ^a   Bennett, Wayne A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WEST FLORIDA   (United States)

Author keywords

Elasmobranch; Gill remodeling; Hematocrit; Hemoglobin; Oxygen

Indexed keywords

HEMOGLOBIN; OXYGEN;

ANALYSIS OF VARIANCE; ANIMAL; ANOXIA; BLOOD; ECOSYSTEM; ELASMOBRANCH; FISH DISEASE; GILL; HEMATOCRIT; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; UNITED STATES; VETERINARY;

ANALYSIS OF VARIANCE; ANIMALS; ANOXIA; ECOSYSTEM; ELASMOBRANCHII; FISH DISEASES; FLORIDA; GILLS; HEMATOCRIT; HEMOGLOBINS; OXYGEN;

EID: 84903527237     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-013-9901-8     Document Type: Article

References (75)

1. Allen TB (1999) The shark almanac. The Lyons Press, New York.
2. Beitinger TL, McCauley RW (1990) Whole-animal physiological processes for the assessment of stress in fishes. J Great Lakes Res 16: 542-575.
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: 84-87.
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: 132-143.
5. Cain DK, Harms CA, Segars A (2004) Plasma biochemistry reference values of wild-caught southern stingrays (Dasyatis americana). J Zoo Wildl Med 35: 471-476.
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: 505-519.
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: 15-26.
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: 287-294.
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: 387-393.
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 Technology.
11. Craig PM, Wood CM, McClelland GB (2007) Gill membrane remodeling with soft-water acclimation in zebrafish (Danio rerio). Physiol Genom 30: 53-60.
12. Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78: 195-207.
13. Fangue NA, Bennett WA (2003) Thermal tolerance responses of laboratory-acclimated and seasonally acclimatized Atlantic stingray, Dasyatis sabina. Copeia 2003: 315-325.
14. Farrell AP (1993) Cardiovascular system. In: Evans DH (ed) The physiology of Fishes. CRC Press, Boca Raton.
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 Florida.
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: 311-321.
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: 349-357.
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: 1701-1710.
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: 2080-2088.
20. Gilbert CR, Williams JD (2002) National Audubon Society field guide to fishes. Alfred Knopf, New York.
21. Gonzalez RJ, McDonald DG (1992) The relationship between oxygen consumption and ion loss in a freshwater fish. J Exp Biol 163: 317-332.
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: 1409-1417.
23. Gudger EW (1946) Does the stingray strike and poison fishes? Sci Mon 63: 110-116.
24. Gunter G (1967) Vertebrates in hypersaline waters. Contr Mar Sci 12: 230-241.
25. Hall FG, Gray IE (1929) The hemoglobin concentration of the blood of marine fishes. J Biol Chem 81: 589-594.
26. Holeton GF, Randall DJ (1967) Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46: 297-305.
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: 61-67.
28. Hughes GM (1984) Measurement of gill area in fishes: practices and problems. J Exp Mar Biol Ass UK 64: 637-655.
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: 74-88.
30. Kajiura S, Tricas T (1996) Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina. J Exp Biol 199: 2297-2306.
31. Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc 276: 735-744.
32. McLeod TF, Sigel MM, Yunis AA (1978) Regulation of erythropoiesis in the Florida gar Lepisosteus platyrhincus. Comp Biochem Physiol A Physiol 60: 145-150.
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: 2016-2027.
34. Muir BS, Hughes GM (1969) Gill dimensions for three species of tunny. J Exp Biol 51: 271-285.
35. Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288: R1079-R1090.
36. Nilsson GE (2007) Gill remodeling in fish-a new fashion or an ancient secret? J Exp Biol 210: 2403-2409.
37. Nilsson GE, Östlund-Nilsson S (2008) Does size matter for hypoxia tolerance in fish? Biol Rev 83: 173-189.
38. Nilsson GE, Dymowska A, Stecyk JAW (2012) New insights into the plasticity of gill structure. Respir Physiol Neuro 184: 214-222.
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: 1109-1115.
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 Sciaenopsocellatus. Mar Ecol Prog 321: 41-53.
41. Perry SF, McDonald DG (1993) Gas exchange. In: Evans DH (ed) The physiology of Fishes. CRC Press, Boca Raton.
42. Perry SF, Jonz MG, Gilmour KM (2009) Chapter 5: oxygen sensing and the hypoxic ventilatory response. Fish Physiol 27: 193-253.
43. Powers DA, Dalessio PM, Lee E, DiMichele L (1986) The molecular ecology of Fundulus heteroclitus hemoglobin-oxygen affinity. Am Zool 26: 235-248.
44. Prosser CL (1991) Comparative animal physiology. Wiley-Liss, Danvers.
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: 273-282.
46. Randall JE (1967) Food habitats of reef fishes of the West Indies. Stud Trop Ocean Miami 5: 665-847.
47. Randall D (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100: 275-288.
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: 313-321.
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: 177-186.
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: 55-58.
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: 1423-1430.
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: e15.
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: 239-251.
54. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge.
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: 1-23.
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: 1818-1829.
57. Smale MA, Rabeni CF (1995) Hypoxia and hyperthermia tolerances of headwater stream fishes. Trans Am Fish Soc 124: 698-710.
58. Snelson FF Jr, Williams-Hooper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatissabina, in Florida coastal lagoons. Copeia 1988: 729-739.
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: 241-251.
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: 3667-3673.
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: 1109-1111.
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: 223-232.
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: 339-348.
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: 239-242.
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: 150-159.
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 Florida.
67. Tunnell JW Jr, Judd FW (2002) The Laguna Madre of Texas and Tamaulipas, 1st edn. Texas A&M University Press, College Station.
68. Tuurala H, Egginton S, Soivio A (1998) Cold exposure increases branchial water-blood barrier thickness in the eel. J Fish Biol 53: 451-455.
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: 297-306.
70. Wallman HL, Bennett WA (2006) Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina. Environ Biol Fish 75: 261-270.
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, Oxford.
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: 109-120.
73. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Philadelphia.
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: 257-276.
75. Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45: 35-45.