Abstract
We investigated the effects of open- and closed-system temperature changes on the O2 affinity of Atlantic bluefin tuna (Thunnus thynnus) blood using in vitro methods essentially identical to those previously employed on tropical tuna species. Bluefin tuna blood has a general O2 affinity (P 50 = 2.6–3.1 kPa or 19–23 mm Hg at 0.5% CO2) similar to that of skipjack tuna, yellowfin tuna, and kawakawa blood (P 50 = 2.8–3.1 kPa at 0.5% CO2) but significantly above that of bigeye tuna blood (P 50 = 1.6–2.0 kPa at 0.5% CO2). We therefore hypothesize that bluefin tuna are less tolerant of hypoxia than bigeye tuna. Further, we found the P 50 of bluefin tuna blood to be slightly reduced by a 10°C open-system temperature increase (e.g., from 4.83 kPa at 15°C to 3.95 kPa at 25°C) and to be completely unaffected by a 10°C closed-system temperature change. Bluefin tuna blood, therefore, had a significantly reduced Bohr effect when subjected to the inevitable changes in P CO 2 and plasma pH that accompany closed-system temperature shifts (0.04–0.09 Δlog P50ΔpH−1) compared with the effects of changes in plasma pH accomplished by changing P CO 2 alone (0.81–0.94 Δlog P50 Δ pH−1). This response is similar to that of skipjack tuna blood, but different from yellowfin or bigeye tuna blood. During closed-system temperature changes at oxygen levels above P 50, however, bluefin tuna blood showed a reversed temperature effect (i.e., P O 2 decreased in response to an increase in temperature). Unlike in other tuna species, temperature effects on O2 affinity of bluefin tuna whole blood were similar to those previously reported for hemoglobin solutions, suggesting that red cell-mediated ligand changes are not involved.
This is a preview of subscription content, access via your institution.




References
Barkley RA, Neill WH, Gooding RM (1978) Skipjack tuna, Katsuwonus pelamis, habitat based on temperature and oxygen requirements. Fish Bull US 76:653–662
Bigelow K, Hampton J, Miyabe N (2002) Application of a habitat-based model to estimate effective longline fishing effort and relative abundance of Pacific bigeye tuna (Thunnus obesus). Fish Oceanogr 11:143–155
Block BA, Keen JE, Castillo B, Dewar H, Freund EV, Marcinek DJ, Brill RW, Farwell C (1997) Environmental preferences of yellowfin tuna (Thunnus albacares) at the northern extent of its range. Mar Biol 130:119–132
Block BA, Dewar H, Blackwell SB, Williams T, Prince E, Boustany AM, Farwell C, Dau DJ, Seitz A (2001a) Archival and pop-up satellite tagging of Atlantic bluefin tuna. In: Sibert J, Neilson J (eds) Methods and technologies in fish biology and fisheries, vol 1. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 65–88
Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, Farwell CJ, Boustany A, Teo SHL, Sietz A, Walli A, Fudge D (2001b) Migratory movements, depth preferences, and the thermal biology of Atlantic bluefin tuna. Science (Washington, DC) 293:1310 –1314
Bourne PK, Cossins AR (1982) On the instability of K+ influx in erythrocytes of rainbow trout, Salmo gairdneri, and the role of catecholamine hormones in maintaining in vivo influx activity. J Exp Biol 101:93–104
Boustany AM, Marcinek D, Keen J, Dewar H, Block BA (2001) Movements and temperature preferences of Atlantic bluefin tuna (Thunnus thynnus) off North Carolina: a comparison of acoustic, archival, and pop-up satellite tags. In: Sibert J, Neilson J (eds) Methods and technologies in fish biology and fisheries, vol 1. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 89–108
Brauner CJ, Randall DJ (1996) The interaction between oxygen and carbon dioxide movements in fishes. Comp Biochem Physiol 113A:83–90
Brill RW (1994) A review of temperature and O2 tolerance studies of tunas pertinent to fisheries oceanography, movement models and stock assessments. Fish Oceanogr 3:204–216
Brill RW, Bushnell PG (1991) Effects of open- and closed-system temperature changes on blood oxygen dissociation curves of skipjack tuna, Katsuwonus pelamis, and yellowfin tuna, Thunnus albacares. Can J Zool 69:1814–1821
Brill RW, Bushnell PG (2001) The cardiovascular system of tunas. In: Block BA, Stevens ED (eds) Fish physiology, vol 19. Tuna—physiology, ecology and evolution. Academic Press, San Diego, pp 79–120
Brill R, Lutcavage M (2001) Understanding environmental influences on movements and depth distribution of tunas and billfish can significantly improve stock assessments. In: Sedberry GR (eds) Island in the stream: oceanography and fisheries of the Charleston Bump. American Fisheries Society, Symposium 25, Bethesda, Maryland, pp 179–198
Brill RW, Bushnell PG, Jones DR, Shimazu M (1992) Effects of acute temperature change, in vivo and in vitro, on the acid–base status of blood from yellowfin tuna (Thunnus albacares). Can J Zool 70:654–662
Brill RW, Cousins KL, Jones DR, Bushnell PG, Steffensen JF (1998) Blood volume, plasma volume and circulation time in a high-energy-demand teleost, the yellowfin tuna (Thunnus albacares). J Exp Biol 201:647–654
Brill R, Lutcavage M, Metzger G, Bushnell P, Arndt M, Lucy J, Watson C (2002) Horizontal and vertical movements of juvenile bluefin tuna (Thunnus thynnus) in the western north Atlantic determined using ultrasonic telemetry. Fish Bull US 100:155–167
Brittain T (1987) The Root effect. Comp Biochem Physiol B 88:473–481
Bushnell PG, Brill RW (1992) Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia. J Comp Physiol 162:131–143
Bushnell PG, Jones DR (1994) Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates. Environ Biol Fishes 40:303–318
Bushnell PG, Brill RW, Bourke RE (1990) Cardiorespiratory responses of skipjack tuna Katsuwonus pelamis; yellowfin tuna, Thunnus albacares; and bigeye tuna, T. obesus, to acute reductions in ambient oxygen. Can J Zool 68:1857–1865
Cameron JN (1971) Rapid method for determination of total carbon dioxide in small blood samples. J Appl Physiol 31:632–634
Carey FG (1973) Fishes with warm bodies. Sci Am 228:36–44
Carey FG, Gibson QH (1977) Reverse temperature dependence of tuna hemoglobin oxygenation. Biochem Biophysic Res Commun 78:1376–1382
Carey FG, Gibson QH (1983) Heat and oxygen exchange in the rete mirable of the bluefin tuna, Thunnus thynnus. Comp Biochem Physiol 74A:333–342
Carey FG, Teal JM (1966) Heat conservation in tuna fish muscle. Proc Natl Acad Sci U S A 56:1461–1469
Carey FG, Kanwisher JW, Stevens ED (1984) Bluefin tuna warm their viscera during digestion. J Exp Biol 109:1–20
Carey FG, Casey JG, Pratt HL, Urquhart D, McCosker JE (1985) Temperature, heat production and heat exchange in lamnid sharks. Mem South Cal Acad Sci 9:92–108
Cayré P, Marsac F (1993) Modeling the yellowfin tuna (Thunnus albacares) vertical distribution using sonic tagging results and local environmental parameters. Aquat Living Resour 6:1–14
Cech JJ, Jr, Laurs RM, Graham JB (1984) Temperature-induced changes in blood gas equilibria in the albacore, Thunnus alalunga, a warm-bodied tuna. J Exp Biol 109:21–34
Dacie JV, Lewis SN (1984) Practical hematology. 5th edn. Churchill Livingstone, Edinburgh
Dalessio PM, DiMichele L, Powers D (1991) Adrenergic effects on the oxygen affinity and pH of cultured erythrocytes and blood of the mummichog, Fundulus heteroclitus. Physiol Zool 64:1407–1425
Gallardo Romero M, Guizouarn H, Pellissier B, Garcia-Romeu F, Motais R (1996) The erythrocyte Na+/H+ exchangers of eel (Anguilla anguilla) and rainbow trout (Onchorynchus mykiss): a comparative study. J Exp Biol 199:415–426
Ganong WF (1973) Review of medical physiology. Lange Medical Publications, Los Altos California
Gilmour KM, Didyk NE, Reid SG, Perry SF (1994) Down-regulation of red blood cell-adrenoreceptors in response to chronic elevation of plasma catecholamine levels in the rainbow trout. J Exp Biol 186:309–314
Godsil HC, Byers RD (1944) A systematic study of the Pacific tunas. Calif Dept Fish Game Fishery Bull 60:1–131
Gooding RG, Neill WH, Dizon AE (1981) Respiration rates and low-oxygen tolerance limits in skipjack tuna, Katsuwonus pelamis. Fish Bull US 79:31–47
Graham JB, Dickson KA (2001) Anatomical and physiological specializations for endothermy. In: Block BA, Stevens ED (eds) Fish physiology, vol 19. Tuna—physiology, ecology and evolution. Academic Press, San Diego, pp 121–166
Graham JB, Dickson KA (2004) Tuna comparative physiology. J Exp Biol 207:4015– 4024
Grigg GC (1969) Oxygen equilibrium curve of the blood of the brown bullhead, Ictacurus nebulosus. Comp Biochem Physiol 29:1203–1223
Gunn J, Block BA (2001) Advances in acoustic, archival, and satellite tagging of tunas. In: Block BA, Stevens ED (eds) Fish physiology, vol 19, Tuna—physiology, ecology and evolution. Academic Press, San Diego, pp 167–224
Hanamoto E (1987) Effect of oceanographic environment on bigeye tuna distribution. Bull Japan Soc Fish Oceanogr 51:203 –216
Hochachka P, Somero G (1984) Biochemical adaptation. Princeton University Press, Princeton New Jersey
Holland K, Brill R, Chang R, Sibert J, Fournier D (1992) Physiological and behavioral thermoregulation in bigeye tuna (Thunnus obesus). Nature 358:410–412
Ikeda-Saito M, Yonetani T, Gibson QH (1983) Oxygen equilibrium studies on hemoglobin from the bluefin tuna (Thunnus thynnus). J Mol Biol 168:673–686
Ingham MC, Cook SK, Hausknecth KA (1977) Oxygen characteristics and skipjack tuna distribution in the southeastern tropical Atlantic. Fish Bull US 75:857–865
Jensen FB, Nikinmaa M, Weber RE (1993) Environmental perturbations of oxygen transport in teleost fishes: causes, consequences and compensations. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 161–179
Jensen FB, Fago A, Weber RW (1998) Hemoglobin structure and function. In: Perry SF, Tufts BL (eds) Fish physiology, vol 17. Academic Press, San Diego, pp 1–40
Jones DR, Brill RW, Mense DC (1986) The influence of blood gas properties on gas tensions and pH of ventral and dorsal aortic blood in free-swimming tuna, Euthynnus affinis. J Exp Biol 120:201–213
Kaloyianni M, Rasidaki A (1996) Adrenergic responses of R. ridibunda red cells. J Exp Zool 276:175–185
Korsmeyer KE, Lai NC, Shadwick RE, Graham JB (1997) Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna, Thunnus albacares. J Exp Biol 200:1987–1997
Larsen C, Male H, Weber RE (2003) ATP-induced reverse temperature effect in isohemoglobins from the endothermic porbeagle shark (Lamna nasus). J Biol Chem 278:30741–30747
Lowe T, Brill R, Cousins K (2000) Blood O2-binding characteristics of bigeye tuna (Thunnus obesus), a high-energy-demand teleost that is tolerant of low ambient O2. Mar Biol 136:1087–1098
Lutcavage ME, Brill RW, Skomal GB, Chase BC, Goldstein JL, Tutein J (2000) Tracking adult northern bluefin tuna (Thunnus thynnus) in the northwestern Atlantic using ultrasonic telemetry. Mar Biol 137:347–358
Lykkeboe G, Weber RE (1978) Changes in the respiratory properties of the blood in the carp, Cyrprinus carpio, induced by diurnal variation in ambient oxygen. J Comp Physiol B 128:117–125
Mathieu-Costello O, Agey PJ, Logermann RB, Brill RW, Hochacka PW (1992) Capillary–fiber geometrical relationships in tuna red muscle. Can J Zool 70:1281–1229
Mohri ME, Hanamoto E, Takeuchi S (1996) Optimum water temperatures for bigeye tuna in the Indian Ocean as seen from tuna longline catches. Nippon Suisan Gakk 63:761–764
Neill WH, Chang RKC, Dizon AE (1976) Magnitude and ecological implications of thermal inertia in skipjack tuna, Katsuwonus pelamis (Linnaeus). Environ Biol Fishes 1:61–80
Nikinmaa M (1990) Vertebrate red blood cells. Springer, New York
Oswald RL (1978) Injection anaesthesia for experimental studies in fish. Comp Biochem Physiol C 60:19–26
Perry SF, Daxboeck C, Emmett B, Hochachka PW, Brill RW (1985) Effects of temperature change on acid–base regulation in skipjack tuna (Katsuwonus pelamis) blood. Comp Biochem Physiol A 81:49–53
Powers DA (1980) Molecular ecology of teleost fish hemoglobins: strategies for adapting to changing environments. Am Zool 19:211–224
Powers DA (1985) Molecular and cellular adaptations of fish hemoglobin–oxygen affinity to environmental changes. In: Lamy J, Truchot J-P, Gilles R (eds) Respiratory pigments in animals. Springer, Berlin, pp 98–124
Powers DA, Martin JP, Garlick RL, Fyhn HJ (1979) The effect of temperature on the oxygen equilibria of fish hemoglobins in relation to thermal variability. Comp Biochem Physiol A 62:87–94
Roig T, Sanchez J, Tort L, Altimiras J, Bermudez J (1997) Adrenergic stimulation of sea bream (Sparus aurata) red blood cells in normoxia and anoxia: effects on metabolism and on the oxygen affinity of haemoglobin. J Exp Biol 200:953–961
Rossi-Fanelli A, Antonini E (1960) Oxygen equilibrium of hemoglobin from Thunnus thynnus. Nature 186:895–896
Sharp GD (1978) Behavioral and physiological properties of tunas and their effects on vulnerability to fishing gear. In: Sharp GD, Dizon AE (eds) The physiological ecology of tunas. Academic Press, New York, pp 397–449
Stokesbudy MJW, Teo SLH, Siez A, O’Dor R, Block BA (2004) Movements of Atlantic bluefin tuna (Thunnus thynnus) as determined by satellite tagging experiments initiated off New England. Can J Fish Aquat Sci 61:1976–1987
Sund PN, Blackburn B, Williams F (1981) Tunas and their environment in the Pacific Ocean: a review. Oceanogr Mar Biol Ann Rev 19:443–512
Truchot J-P (1987) Comparative aspects of extracellular acid–base balance. Springer, New York
Tucker VA (1967) Method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:410–414
Wells RMG, McIntyre RH, Morgan AK, Davie PS (1986) Physiological stress response in big gamefish after capture: observations on plasma chemistry and blood factors. Comp Physiol Biochem A 84:565 – 571
Wood SC (1980) Adaptations of red blood cell function to hypoxia and temperature in ectothermic vertebrates. Am Zool 20:163–172
Yang T-H, Lai NC, Graham JB, Somero GN (1992) Respiratory, blood, and heart enzymatic adaptations of Sebastolobus alascanus (Scorpaenidae;Teleostei) to the oxygen minimum zone: a comparative study. Biol Bull Mar Biol Lab Woods Hole 183:490–499
Acknowledgments
This research was supported by the National Marine Fisheries Service (Northeast Fisheries Science Center), a partial IUSB faculty research grant (PGB), and NOAA Grant NA04NMF4550391 to the Large Pelagics Research Center–University of New Hampshire. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its sub-agencies. The experiments, animal maintenance, anesthesia, and animal handling procedures described herein were approved by the College and William and Mary Institutional Animal Care and Use Committee and comply with all current applicable laws of the United States of America. The authors gratefully acknowledge Jack Stallings, Molly Lutcavage, John Logan, Roy Pemberton, and Andrij Horodysky for collecting live tunas and for their help during the experiments. We especially thank Mark Luckenbach, Reade Bonniwell, and the staff of the Virginia Institute of Marine Science Eastern Shore Laboratory for their continuing and genuine hospitality and for providing both fish holding and laboratory facilities. This is contribution 2761 from the Virginia Institute of Marine Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Brill, R.W., Bushnell, P.G. Effects of open- and closed-system temperature changes on blood O2-binding characteristics of Atlantic bluefin tuna (Thunnus thynnus). Fish Physiol Biochem 32, 283–294 (2006). https://doi.org/10.1007/s10695-006-9104-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-006-9104-7
Keywords
- Cardiorespiratory
- Fish
- Hemoglobin
- Hypoxia
- Pelagic
- Metabolic rate
- Oxygen affinity
- Scrombridae