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Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 949–967 | Cite as

Temperature effects on the blood oxygen affinity in sharks

  • Diego Bernal
  • Joseph P. Reid
  • Julie M. Roessig
  • Shinsyu Matsumoto
  • Chugey A. Sepulveda
  • Joseph J. CechJr.
  • Jeffrey B. Graham
Article

Abstract

In fish, regional endothermy (i.e., the capacity to significantly elevate tissue temperatures above ambient via vascular heat exchangers) in the red swimming muscles (RM) has evolved only in a few marine groups (e.g., sharks: Lamnidae, Alopiidae, and teleosts Scombridae). Within these taxa, several species have also been shown to share similar physiological adaptations to enhance oxygen delivery to the working tissues. Although the hemoglobin (Hb) of most fish has a decreased affinity for oxygen with an increase in temperature, some regionally endothermic teleosts (e.g., tunas) have evolved Hbs that have a very low or even an increased affinity for oxygen with an increase in temperature. For sharks, however, blood oxygen affinities remain largely unknown. We examined the effects of temperature on the blood oxygen affinity in two pelagic species (the regionally endothermic shortfin mako shark and the ectothermic blue shark) at 15, 20, and 25 °C, and two coastal ectothermic species (the leopard shark and brown smooth-hound shark) at 10, 15, and 20 °C. Relative to the effects of temperature on the blood oxygen affinity of ectothermic sharks (e.g., blue shark), shortfin mako shark blood was less affected by an increase in temperature, a scenario similar to that documented in some of the tunas. In the shortfin mako shark, this may act to prevent premature oxygen dissociation from Hb as the blood is warmed during its passage through vascular heat exchangers. Even though the shortfin mako shark and blue shark occupy a similar niche, the effects of temperature on blood oxygen affinity in the latter more closely resembled that of the blood in the two coastal shark species examined in this study. The only exception was a small, reverse temperature effect (an increase in blood oxygen affinity with temperature) observed during the warming of the leopard shark blood under simulated arterial conditions, a finding that is likely related to the estuarine ecology of this species. Taken together, we found species-specific differences in how temperature affects blood oxygen affinity in sharks, with some similarities between the regionally endothermic sharks and several regionally endothermic teleost fishes.

Keywords

Hemoglobin Temperature effects Elasmobranchs Regional endothermy Ectothermy 

Notes

Acknowledgements

We thank S. Matern for the help with coastal sharks collection; J. Clegg, P. Siri, K. Brown, K. Briggman, and W. Borgeson for the facilities and animal care help at the BML; C. Crocker and H. Boyle for the experimental technique help; R. Kaufman, J. Poletto, and D. Cocherell for the statistical assistance; and P. Cala and J. Payne for the comments on drafts of the manuscript. We thank the three anonymous reviewers for their thoughtful comments and suggestions, which significantly improved the quality of this manuscript.

Funding

We are indebted to T. Tazo, S. Malt, J. Valdez, and T. Reposado, for logistical support. Research was funded via a BML Intercampus Travel Grant to JPR, and a Hatch grant (No. 3455-H) to JJC. This material is based in part upon work supported by the National Science Foundation under Grant Number IOS-1354593 and IOS-1354772. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. We dedicate this work to “Grandpa” Jeff; he will be missed but not forgotten.

References

  1. Ackerman JT, Kondratieff MC, Matern SA, Cech JJ (2000) Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata, in Tomales Bay, California. Environ Biol Fish 58:33–43CrossRefGoogle Scholar
  2. Alexander N, Laurs RM, McIntosh A, Russell SW (1980) Haematological characteristics of albacore Thunnus alalunga (Bonnaterre) and skipjack Katsuwonus pelamis (Linnaeus). J Fish Biol 16:383–395CrossRefGoogle Scholar
  3. Andersen ME, Olson JS, Gibson QH (1973) Studies on ligand binding to hemoglobins from teleosts and elasmobranchs. J Biol Chem 10:331–341Google Scholar
  4. Anderson SA, Goldman KJ (2001) Temperature measurements from salmon sharks, Lamna ditropis, in Alaskan waters. Copeia 2001:794–796CrossRefGoogle Scholar
  5. Bernal D, Lowe, C (2015) Field studies of elasmobranch physiology. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Fish physiology. Physiology of elasmobranch fishes. Part A. vol 34. Academic Press, pp. 311-377Google Scholar
  6. Bernal D, Dickson KA, Shadwick RE, Graham JB (2001a) Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comp Biochem Physiol A 129:695–726CrossRefGoogle Scholar
  7. Bernal D, Sepulveda C, Graham JB (2001b) Water-tunnel studies of heat balance in swimming mako sharks. J Exp Biol 204:4043–4054PubMedGoogle Scholar
  8. Bernal D, Smith D, Lopez G, Weitz D, Grimminger T, Dickson K, Graham JB (2003) Comparative studies of high performance swimming in sharks. II. Metabolic biochemistry of locomotor and myocardial muscle in endothermic and ectothermic sharks. J Exp Biol 206:2845–2857CrossRefPubMedGoogle Scholar
  9. Bernal D, Donley JM, Shadwick RE, Syme DA (2005) Mammal-like muscles power swimming in a cold-water shark. Nature 437:1349–1351CrossRefPubMedGoogle Scholar
  10. Bernal D, Sepulveda C, Musyl M, Brill R (2009) The eco-physiology of swimming and movement patterns of tunas, billfishes, and large pelagic sharks. In: Domenici P, Kapoor D (eds) Fish locomotion—an etho-ecological approach. Enfield Scientific Publishers, Enfield, NH, p 436–483Google Scholar
  11. Bernal D, Brill RM, Dickson KA, Shiels HA (2017) Sharing the water column: physiological mechanisms underlying species-specific habitat use in tunas. Rev Fish Biol Fish 27:843–880CrossRefGoogle Scholar
  12. Boutilier RG, Heming TA, Iwama GK (1984) Appendix: physiochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall DJ (eds) Fish physiology. Gills. Part A: anatomy, gas transfer, and acid base regulation, vol. 10. Academic Press, New York, pp 403–430CrossRefGoogle Scholar
  13. Brill RW (1996) Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish. Comp Biochem Physiol A 113:3–15CrossRefGoogle Scholar
  14. Brill RW, Bushnell PG (1991) Effects of open- and closed-system temperature changes on blood dissociation curves of skipjack tuna, Katsuwonus pelamis, and yellowfin tuna, Thunnus albacares. Can J Zool 69:1814–1821CrossRefGoogle Scholar
  15. Brill RW, Bushnell PG (2006) Effects of open- and closed-system temperature changes on blood-O2 binding characteristics of Atlantic bluefin tuna (Thunnus thynnus). Fish Physiol Biochem 32:283–294CrossRefGoogle Scholar
  16. Brill RW, Block BA, Boggs CH, Bigelow KA, Freund EV, Marcinek DJ (1999) Horizontal movements and depth distribution of large adult yellowfin tuna (Thunnus albacares) near the Hawaiian islands, recoded using ultrasonic telemetry: implications for the physiological ecology of pelagic fishes. Mar Biol 133:395–408CrossRefGoogle Scholar
  17. 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 the sandbar shark (Carcharhinus plumbeus Nardo). J Exp Mar Biol Ecol 354:132–143CrossRefGoogle Scholar
  18. Butler PJ, Metcalfe JD (1988) Cardiovascular and respiratory systems. In Shuttlewroth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, Heidelberg. pp. 1-47.Google Scholar
  19. Campos BR, Fish MA, Jones G, Riley RW, Allen PJ, Klimley AP, Cech JJ, Kelly JT (2009) Movements of brown smooth-hounds in Tomales Bay, California. Environ Biol Fish 85:3–13CrossRefGoogle Scholar
  20. Carey FG, Gibson QH (1977) Reverse temperature dependence of tuna hemoglobin oxygenation. Biochem Biophys Res Commun 78:1376–1382CrossRefPubMedGoogle Scholar
  21. Carey FG, Scharold JV (1990) Movements of blue sharks, Prionace glauca, in depth and course. Mar Biol 106:329–342CrossRefGoogle Scholar
  22. Carey FG, Teal JM (1969) Mako and porbeagle: warm bodied sharks. Comp Biochem Physiol A 28:199–204CrossRefGoogle Scholar
  23. Carey FG, Teal JM, Kanwisher JW, Lawson KD, Beckett JS (1971) Warm-bodied fish. Am Zool 11:135–143CrossRefGoogle Scholar
  24. Carey FG, Teal JM, Kanwisher JW (1981) The visceral temperatures of mackerel sharks (Lamnidae). Physiol Zool 54:334–344CrossRefGoogle Scholar
  25. Carey FG, Casey JG, Pratt HL, Urquhart D, McCosker JE (1985) Temperature, heat production and heat exchange in lamnid sharks. Mem So Calif Acad Sci 9:92–108Google Scholar
  26. Cech JJ, Laurs RM, Graham JB (1984) Temperature-induced changes in blood gas equilibria in the albacore, Thunnus alalunga, a warm-bodied tuna. J Exp Biol 109:92–108Google Scholar
  27. Clauvel M, Schwartz K (1968) Blood oxygen capacity: technical difficulties of its determination by the Van Slyke method and comparison with hemoglobin content. Clin Chem 14:253–261PubMedGoogle Scholar
  28. Cliff G, Thurman GD (1984) Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp Biochem Physiol 78A:167–173CrossRefGoogle Scholar
  29. Cooper AR, Morris S (2004) Hemoglobin function and respiratory status of the Port Jackson shark, Heterodontus portusjacksoni, in response to lowered salinity. J Comp Physiol B 174:223–236CrossRefPubMedGoogle Scholar
  30. Davenport HW (1974) The ABC of acid-base chemistry. University of Chicago Press, ChicagoGoogle Scholar
  31. Dewar H, Graham JB (1994) Studies of tropical tuna swimming performance in a large swimming tunnel: I. Energetics. J Exp Biol 192:13–31PubMedGoogle Scholar
  32. Dickson KA, Graham JB (2004) Evolution and consequences of endothermy in fishes. Physiol Biochem Zool 77:998–1018CrossRefPubMedGoogle Scholar
  33. Edwards MJ, Martin RJ (1966) Mixing technique for the oxygen-hemoglobin equilibrium and Bohr effect. J Appl Physiol 21:1898–1902CrossRefPubMedGoogle Scholar
  34. Emery SH (1985) Hematology and cardiac morphology in the great white shark, Carcharodon carcharias. So Calif Acad Sci Mem 9:73–80Google Scholar
  35. Emery SH (1986) Hematological comparisons of endothermic vs. ectothermic elasmobranch fishes. Copeia 1996:700–705CrossRefGoogle Scholar
  36. Graham JB, Dickson KA (2004) Tuna comparative physiology. J Exp Biol 207:4015–4024CrossRefPubMedGoogle Scholar
  37. Graham JB, Dewar H, Lai NC, Lowell WR, Arce SM (1990) Aspects of shark swimming performance determined using a large water tunnel. J Exp Biol 151:175–192Google Scholar
  38. Haeseker SL, Cech JJ (1993) Food habits of the brown smooth-hound shark (Mustelus henlei) from two sites in Tomales Bay. Calif Fish Game 79:89–95Google Scholar
  39. Hall FG (1960) A tonometric apparatus for constant flow gas equilibrium. J Appl Physiol 15:312–313CrossRefPubMedGoogle Scholar
  40. Harms T, Ross T, Segars A (2002) Plasma biochemistry reference values for wild bonnethead sharks Sphyrna tiburo. Vet Clin Pathol 31:111–115CrossRefPubMedGoogle Scholar
  41. Hight BV, Lowe CG (2007) Elevated body temperatures of female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence of behavioral thermoregulation? J Exp Mar Biol Ecol 352:114–128CrossRefGoogle Scholar
  42. Hoar WS, Hickman CP (1983) A laboratory companion for general and comparative physiology. Prentice Hall, New Jersey, p 340Google Scholar
  43. Holts DB, Bedford DW (1993) Horizontal and vertical movements of the shortfin mako, Isurus oxyrinchus, in the Southern California Bight. Aust J Mar Freshwat Res 44:45–60CrossRefGoogle Scholar
  44. Hopkins TE, Cech JJ (1994) Temperature effects of blood-oxygen equilibria in relation to movements of the bat ray, Myliobatis californica, in Tomales Bay, California. Mar Behav Physiol 24:227–235CrossRefGoogle Scholar
  45. Hopkins TE, Cech JJ (2003) The influence of environmental variables on the distribution and abundance of elasmobranch fishes in Tomales Bay, California. Environ Biol Fish 66:279–291CrossRefGoogle Scholar
  46. Howell BJ, Baumgardner FW, Bondi K, Rahn F (1970) Acid-base balance in cold-blooded vertebrates as a function of body temperature. Am J Phys 218:600–606Google Scholar
  47. Jensen FB (1991) Multiple strategies in oxygen and carbon dioxide transport by haemoglobin. In: Woakes J, Grieshaber MK, Bridges CR (eds) Physiological strategies for gas exchange and metabolism. Cambridge University Press, Cambridge, pp 55–78Google Scholar
  48. Kaufman RC, Houck AG, Cech JJ (2006) Effects of temperature and carbon dioxide on green sturgeon blood-oxygen equilibria. Environ Biol Fish 76:119–127CrossRefGoogle Scholar
  49. Lai NC, Graham JB, Burnett L (1990) Blood respiratory properties and the effect of swimming on blood gas transport in the leopard shark Triakis semifasciata. J Exp Biol 151:161–173Google Scholar
  50. Larsen C, Malte H, Weber RE (2003) ATP-induced reverse temperature effect in iso-hemoglobins from the endothermic porbeagle shark, Lamna nasus. J Biol Chem 278:30741–30747CrossRefPubMedGoogle Scholar
  51. Loefer JK, Sedberry GR, McGovern JC (2005) Vertical movements of a shortfin mako in the western North Atlantic as determined by pop-up satellite tagging. Southeast Nat 4:237–246CrossRefGoogle Scholar
  52. Love M (1996) Probably more than you want to know about the fishes of the Pacific coast, 2nd edn. Really Big Press, Santa Barbara 335 pGoogle Scholar
  53. Lowe TE, Brill RW, Cousins KL (2000) Blood oxygen-binding characteristics of bigeye tuna (Thunnus obesus), a high-energy-demand teleost that is tolerant to low ambient oxygen. Mar Biol 136:1087–1098CrossRefGoogle Scholar
  54. Mandelman JW, Skomal GB (2009) Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks. J Comp Physiol B 179:367–277CrossRefGoogle Scholar
  55. Matern SA, Cech JJ, Hopkins TE (2000) Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation? Environ Biol Fish 58:173–182CrossRefGoogle Scholar
  56. Miklos P, Katzman SM, Cech JJ (2003) Effect of temperature on oxygen consumption of the leopard shark, Triakis semifasciata. Environ Biol Fish 66:15–18CrossRefGoogle Scholar
  57. Miller DJ, Lea RN (1972) Guide to the coastal marine fishes of California: California Fish Bulletin Number 157. Division of Agricultural Sciences, University of California, RichmondGoogle Scholar
  58. Morrison PR, Gilmour KM, Brauner CJ (2015). Oxygen and carbon dioxide transport in elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Fish physiology. Physiology of elasmobranch fishes. Part B. vol 34. Academic Press, pp. 127–219Google Scholar
  59. Mumm DP, Atha DH, Riggs A (1978) The hemoglobin of the common sting-ray, Dasyatis sabina: structural and functional properties. Comp Biochem Physiol B 60:189–193CrossRefPubMedGoogle Scholar
  60. Nikinmaa M (1990) Oxygen Transport. In: Vertebrate Red Blood Cells. Zoophysiology, vol 28. Springer, Berlin, HeidelbergCrossRefGoogle Scholar
  61. Nikinmaa M, Salama A (1998) Oxygen transport in fish. In: Perry SF, Tufts BL (eds) Fish physiology. Fish respiration, vol 17. Academic Press, San Diego, pp 141–184Google Scholar
  62. Powers DA, Martin JP, Garlick RL, Fyhn HJ, Fyhn UEH (1979) The effect of temperature on the oxygen equilibria of fish hemoglobins in relation to environmental thermal variability. Comp Biochem Physiol A 62:87–94CrossRefGoogle Scholar
  63. Reeves RB (1976) Temperature-induced changes in blood acid-base status: pH and PCO2 in a binary buffer. J Appl Physiol 40:752–761CrossRefPubMedGoogle Scholar
  64. Riggs A (1970) Properties of fish hemoglobins. In: Hoar WS, Randall DJ (eds) Fish physiology. the nervous system, circulation, and respiration, vol 4. Academic Press, New York, pp 209–252CrossRefGoogle Scholar
  65. Root RW (1931) The respiratory function of the blood of marine fishes. Biol Bull 61:427–456CrossRefGoogle Scholar
  66. Rossi-Fanelli A, Antonini E (1960) Oxygen equilibrium of hemoglobin from Thunnus thynnus. Nature 186:895–896CrossRefPubMedGoogle Scholar
  67. Schaefer KM, Fuller DW, Block BA (2007) Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data. Mar Biol 52:503–525CrossRefGoogle Scholar
  68. Scheid P, Meyer M (1978) Mixing technique for study of oxygen-hemoglobin equilibrium: a critical evaluation. J Appl Physiol Respir Environ Exerc Physiol 45:818–822PubMedGoogle Scholar
  69. Sepulveda CA, Kohin S, Chan C, Vetter R, Graham JB (2004) Movement patterns, depth preferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Mar Biol 145:191–199CrossRefGoogle Scholar
  70. Sepulveda CA, Graham JB, Bernal D (2007) Aerobic metabolic rates of swimming juvenile mako sharks, Isurus oxyrinchus. Mar Biol 152:1087–1094CrossRefGoogle Scholar
  71. Setka JD, Cech JJ (1994) Blood and muscle characteristics of leopard shark (Triakis semifasciata) and brown smooth-hound (Mustelus henlei). Calif Fish Game 80:89–96Google Scholar
  72. Sharp GD (1975) A comparison of the O2 dissociation properties of some scombrid hemoglobins. Comp Biochem Physiol 51A:683–691CrossRefGoogle Scholar
  73. Smith RL, Rhodes D (1983) Body temperature of the salmon shark, Lamna ditropis. J Mar Biol Assoc UK 63:243–244CrossRefGoogle Scholar
  74. Smith SV, Hollibaugh JT, Dollar SJ, Vink S (1991) Tomales Bay metabolism: C-N-P stoichiornetry and ecosystem heterotrophy at the land-sea interface. Estuar Coast Shelf Sci 33:223–257CrossRefGoogle Scholar
  75. Stevens ED, Randall DJ (1967) Changes of gas concentrations in blood and water during moderate swimming activity in rainbow trout. J Exp Biol 46:329–337PubMedGoogle Scholar
  76. Stevens ED, Kanwisher JW, Carey FG (2000) Muscle temperature in free-swimming giant Atlantic bluefin tuna (Thunnus thynnus L.) J Therm Biol 25:419–423CrossRefPubMedGoogle Scholar
  77. Tucker V (1967) Method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:410–414CrossRefPubMedGoogle Scholar
  78. Webber JD, Cech JJ (1998) Non-destructive diet analysis of the leopard shark, Triakis semifasciata, from two sites in Tomales Bay, California. Calif Fish Game 84:18–24Google Scholar
  79. Weber RE (1983) TMAO (trimethylamine-oxide)-independence of oxygen affinity and its urea and ATP sensitivities in an elasmobranch hemoglobin. J Exp Zool 228:551–554CrossRefPubMedGoogle Scholar
  80. Wells RMG, Davie PS (1985) Oxygen binding by the blood and hematological effects of capture stress in two big gamefish: mako shark and striped marlin. Comp Biochem Physiol A 81:643–646CrossRefPubMedGoogle Scholar
  81. Wells RMG, Weber RE (1983) Oxygenational properties and phosphorylated metabolic intermediates in blood and erythrocytes of the dogfish, Squalus acanthus. J Exp Biol 103:95–108PubMedGoogle Scholar
  82. Wood CM, McMahon BR, McDonald DG (1977) An analysis of changes in blood pH following exhausting activity in the starry flounder, Platichthys stellatus. J Exp Biol 69:173–185PubMedGoogle Scholar
  83. Wyman J (1964) Linked functions and reciprocal effects in hemoglobin: a second look. Adv Protein Chem 19:223–286CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Center for Marine Biotechnology and BiomedicineScripps Institution of OceanographyLa JollaUSA
  2. 2.Department of BiologyUniversity of MassachusettsDartmouthUSA
  3. 3.Department of Wildlife, Fish, and Conservation BiologyUniversity of CaliforniaDavisUSA
  4. 4.Pfleger Institute of Environmental ResearchOceansideUSA

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