Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch

Journal of Experimental Biology

Volumn 218, Issue 15, 2015, Pages 2448-2454

  Brijs, Jeroen ^a   Jutfelt, Fredrik ^a   Clark, Timothy D ^b,d   Gräns, Albin ^c   Ekström, Andreas ^a   Sandblom, Erik ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Aerobic scope; Anaemia; Hyperoxia; Metabolism; Oxygen consumption; Temperature

Indexed keywords

HEMOGLOBIN; OXYGEN;

AEROBIC METABOLISM; ANEMIA; ANIMAL; BASAL METABOLIC RATE; HEAT; METABOLISM; OXYGEN CONSUMPTION; PERCH; PHYSIOLOGY;

AEROBIOSIS; ANEMIA; ANIMALS; BASAL METABOLISM; HEMOGLOBINS; HOT TEMPERATURE; OXYGEN; OXYGEN CONSUMPTION; PERCHES;

EID: 84956596297     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.121889     Document Type: Article

References (58)

1. Anttila, K., Dhillon, R. S., Boulding, E. G., Farrell, A. P., Glebe, B. D., Elliott, J. A. K., Wolters, W. R. and Schulte, P. M. (2013). Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level. J. Exp. Biol. 216, 1183-1190.
2. Barrett, D. J. and Taylor, E. W. (1984). Changes in heart rate during progressive hyperoxia in the dogfish Scyliorhinus canicula L.: Evidence for a venous oxygen receptor. Comp. Biochem. Physiol. A Comp. Physiol. 78, 697-703.
3. Beers, J. M. and Sidell, B. D. (2011). Thermal tolerance of Antarctic Notothenioid fishes correlates with level of circulating hemoglobin. Physiol. Biochem. Zool. 84, 353-362.
4. Beitinger, T. L., Bennett, W. A. and McCauley, R. W. (2000). Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ. Biol. Fish. 58, 237-275.
5. Brett, J. R. (1971). Energetic responses of salmon to temperature - study of some thermal relations in physiology and freshwater ecology of Sockeye Salmon (Oncorhynchus Nerka). Amer. Zool. 11, 99-113.
6. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771-1789.
7. Caldeira, K. and Wickett, M. E. (2003). Oceanography: Anthropogenic carbon and ocean pH. Nature 425, 365-365.
8. Cameron, J. N. and Davis, J. C. (1970). Gas exchange in rainbow trout (Salmo gairdneri) with varying blood oxygen capacity. J. Fish. Res. Board Can. 27, 1069-1085.
9. Clark, T. D., Eliason, E. J., Sandblom, E., Hinch, S. G. and Farrell, A. P. (2008). Calibration of a hand-held haemoglobin analyser for use on fish blood. J. Fish Biol. 73, 2587-2595.
10. Clark, T. D., Jeffries, K. M., Hinch, S. G. and Farrell, A. P. (2011). Exceptional aerobic scope and cardiovascular performance of pink salmon (Oncorhynchus gorbuscha) may underlie resilience in a warming climate. J. Exp. Biol. 214, 3074-3081.
11. Clark, T. D., Sandblom, E. and Jutfelt, F. (2013a). Aerobic scope measurements of fishes in an era of climate change: Respirometry, relevance and recommendations. J. Exp. Biol. 216, 2771-2782.
12. Clark, T. D., Sandblom, E. and Jutfelt, F. (2013b). Response to Farrell and to Pörtner and Giomi. J. Exp. Biol. 216, 4495-4497.
13. Cossins, A. R. and Bowler, K. (1987). Temperature Biology of Animals. London: Chapman and Hall.
14. Currie, S., Ahmady, E., Watters, M. A., Perry, S. F. and Gilmour, K. M. (2013). Fish in hot water: Hypoxaemia does not trigger catecholamine mobilization during heat shock in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 165, 281-287.
15. Ekström, A., Jutfelt, F. and Sandblom, E. (2014). Effects of autonomic blockade on acute thermal tolerance and cardioventilatory performance in rainbow trout, Oncorhynchus mykiss. J. Therm. Biol. 44, 47-54.
16. Farrell, A. P. (2013). Aerobic scope and its optimum temperature: Clarifying their usefulness and limitations - correspondence on J. Exp. Biol. 216, 2771-2782. J. Exp. Biol. 216, 4493-4494.
17. Farrell, A. P., Eliason, E. J., Clark, T. D. and Steinhausen, M. F. (2014). Oxygen removal from water versus arterial oxygen delivery: Calibrating the Fick equation in Pacific salmon. J. Comp. Physiol. B 184, 855-864.
18. Fry, F. E. J. (1947). Effects of the environment on animal activity. Publ. Ontario Fish. Res. Lab. 68, 1-62.
19. Fry, F. E. J. (1971). The effect of environmental factors on the physiology of fish. In Fish Physiology, Vol. 6 (ed. W. S. Hoar and D. J. Randall), pp. 1-98. London: Academic Press.
20. Fry, F. E. J. and Hart, J. S. (1948). The relation of temperature to oxygen consumption in the goldfish. Biol. Bull. 94, 66-77.
21. Gallaugher, P. and Farrell, A. P. (1998). Hematocrit and blood oxygen-carrying capacity. In Fish Respiration, Vol. 17 (ed. S. F. Perry and B. Tufts), pp. 185-227. San Diego: Academic Press.
22. Gillooly, J. F., Brown, J. H.,West, G. B., Savage, V. M. and Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science 293, 2248-2251.
23. Glover, C. N., Bucking, C. and Wood, C. M. (2013). The skin of fish as a transport epithelium: A review. J. Comp. Physiol. B 183, 877-891.
24. Gräns, A., Jutfelt, F., Sandblom, E., Jonsson, E., Wiklander, K., Seth, H., Olsson, C., Dupont, S., Ortega-Martinez, O., Einarsdottir, I. et al. (2014). Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut. J. Exp. Biol. 217, 711-717.
25. Harte, J. (2004). The value of null theories in ecology. Ecology 85, 1792-1794.
26. Healy, T. M. and Schulte, P. M. (2012). Factors affecting plasticity in wholeorganism thermal tolerance in common killifish (Fundulus heteroclitus). J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 182, 49-62.
27. Hillebrand, H., Soininen, J. and Snoeijs, P. (2010). Warming leads to higher species turnover in a coastal ecosystem. Glob. Change Biol. 16, 1181-1193.
28. Huey, R. B. and Kingsolver, J. G. (2011). Variation in universal temperature dependence of biological rates. Proc. Natl. Acad. Sci. USA 108, 10377-10378.
29. Huey, R. B., Kearney, M. R., Krockenberger, A., Holtum, J. A. M., Jess, M. and Williams, S. E. (2012). Predicting organismal vulnerability to climate warming: Roles of behaviour, physiology and adaptation. Philos. Trans. R. Soc. B Biol. Sci. 367, 1665-1679.
30. Iftikar, F. I. and Hickey, A. J. R. (2013). Do mitochondria limit hot fish hearts? Understanding the role of mitochondrial function with heat stress in Notolabrus celidotus. Plos ONE 8, e64120.
31. Jutfelt, F., Gräns, A., Jönsson, E.,Wiklander, K., Seth, H., Olsson, C., Dupont, S., Ortega-Martinez, O., Sundell, K., Axelsson, M. et al. (2014). Response to 'How and how not to investigate the oxygen and capacity limitation of thermal tolerance (OCLTT) and aerobic scope - remarks on the article by Gräns et al.'. J. Exp. Biol. 217, 4433-4435.
32. Lannig, G., Bock, C., Sartoris, F. J. and Portner, H. O. (2004). Oxygen limitation of thermal tolerance in cod, Gadus morhua L., studied by magnetic resonance imaging and on-line venous oxygen monitoring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R902-R910.
33. Levitus, S., Antonov, J. I., Boyer, T. P. and Stephens, C. (2000). Warming of the world ocean. Science 287, 2225-2229.
34. Mark, F. C., Bock, C. and Portner, H. O. (2002). Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and P-31-MRS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R1254-R1262.
35. Meehl, G. A. and Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994-997.
36. Norin, T., Malte, H. and Clark, T. D. (2014). Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J. Exp. Biol. 217, 244-251.
37. Olson, K. R. (1992). Blood and extracellular fluid volume regulation: Role of the reninangiotensin system, kallikrein-kinin system, and atrial natriuretic peptides. In Fish Physiology: The Cardiovascular System, Vol. 12B (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 135-254. San Diego, CA: Academic Press, Inc.
38. Overgaard, J., Andersen, J. L., Findsen, A., Pedersen, P. B. M., Hansen, K., Ozolina, K. and Wang, T. (2012). Aerobic scope and cardiovascular oxygen transport is not compromised at high temperatures in the toad Rhinella marina. J. Exp. Biol. 215, 3519-3526.
39. Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637-669.
40. Perry, S. F., Reid, S. G. and Salama, A. (1996). The effects of repeated physical stress on the beta-adrenergic response of the rainbow trout red blood cell. J. Exp. Biol. 199, 549-562.
41. Perry, A. L., Low, P. J., Ellis, J. R. and Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science 308, 1912-1915.
42. Pörtner H. O. (2002). Climate variations and the physiological basis of temperature dependent biogeography: Systemic to molecular hierarchy of thermal tolerance in animals. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132, 739-761.
43. Pörtner, H.-O. (2014). How and how not to investigate the oxygen and capacity limitation of thermal tolerance (OCLTT) and aerobic scope - remarks on the article by Grans et al. J. Exp. Biol. 217, 4432-4433.
44. Pörtner, H. O. and Farrell, A. P. (2008). ECOLOGY: Physiology and climate change. Science 322, 690-692.
45. Pörtner, H.-O. and Giomi, F. (2013). Nothing in experimental biology makes sense except in the light of ecology and evolution - correspondence on J. Exp. Biol. 216, 2771-2782. J. Exp. Biol. 216, 4494-4495.
46. Rutledge, C. J. and Beitinger, T. L. (1989). The effects of dissolved oxygen and aquatic surface respiration on the critical thermal maxima of three intermittentstream fishes. Environ. Biol. Fish. 24, 137-143.
47. Sandstrom, O., Neuman, E. and Thoresson, G. (1995). Effects of temperature on life history variables in perch. J. Fish Biol. 47, 652-670.
48. Sartoris, F. J., Bock, C., Serendero, I., Lannig, G. and Pörtner, H. O. (2003). Temperature-dependent changes in energy metabolism, intracellular pH and blood oxygen tension in the Atlantic cod. J. Fish Biol. 62, 1239-1253.
49. Seneviratne, S. I., Donat, M. G., Mueller, B. and Alexander, L. V. (2014). No pause in the increase of hot temperature extremes. Nat. Clim.Change 4, 161-163.
50. Seth, H., Grans, A., Sandblom, E., Olsson, C., Wiklander, K., Johnsson, J. I. and Axelsson, M. (2013). Metabolic scope and interspecific competition in sculpins of Greenland are influenced by increased temperatures due to climate change. PLoS ONE 8, e62859.
51. Simonot, D. L. and Farrell, A. P. (2007). Cardiac remodelling in rainbow trout (Oncorhynchus mykiss Walbaum) in response to phenylhydrazine-induced anaemia. J. Exp. Biol. 210, 2574-2584.
52. Soncini, R. and Glass, M. L. (1997). The effects of temperature and hyperoxia on arterial PO2 and acid-base status in Piaractus mesopotamicus. J. Fish Biol. 51, 225-233.
53. Steffensen, J. F. (1989). Some errors in respirometry of aquatic breathers: How to avoid and correct for them. Fish Physiol. Biochem. 6, 49-59.
54. Takeda, T. (1990). Ventilation, cardiac output and blood respiratory parameters in the carp, Cyprinus carpio, during hyperoxia. Resp. Physiol. 81, 227-239.
55. Vornanen, M., Haverinen, J. and Egginton, S. (2014). Acute heat tolerance of cardiac excitation in the brown trout (Salmo trutta fario). J. Exp. Biol. 217, 299-309.
56. Wang, T., Lefevre, S., Iversen, N. K., Findorf, I., Buchanan, R. and McKenzie, D. J. (2014). Anaemia only causes a small reduction in the upper critical temperature of sea bass: Is oxygen delivery the limiting factor for tolerance of acute warming in fishes? J. Exp. Biol. 217, 4275-4278.
57. Weatherley, A. H. (1970). Effects of superabundant oxygen on thermal tolerance of goldfish. Biol. Bull. 139, 229.
58. Zakhartsev, M. V., De Wachter, B., Sartoris, F. J., Portner, H. O. and Blust, R. (2003). Thermal physiology of the common eelpout (Zoarces viviparus). J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 173, 365-378.