Responses to temperature and hypoxia as interacting stressors in fish: Implications for adaptation to environmental change

Integrative and Comparative Biology

Volumn 53, Issue 4, 2013, Pages 648-659

  McBryan, T L ^a   Anttila, K ^a   Healy, T M ^a   Schulte, P M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ENVIRONMENT; FISH; HUMAN ACTIVITIES; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SPECIES DIFFERENCE; TEMPERATURE;

ADAPTATION, BIOLOGICAL; ANIMALS; ENVIRONMENT; FISHES; HUMAN ACTIVITIES; MODELS, BIOLOGICAL; OXYGEN; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; TEMPERATURE;

EID: 84885052783     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/ict066     Document Type: Article

References (78)

1. Alabaster J, Welcomme R. 1962. Effect of concentration of dissolved oxygen on survival of trout and roach in lethal temperatures. Nature 194:107.
2. Anttila K, Dhillon RS, Boulding EG, Farrell AP, Glebe BD, Elliott JAK, Wolters WR, Schulte PM. 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 216:1183-90.
3. Baroudy E, Elliott J. 1994. The critical thermal limits for juvenile Arctic charr Salvelinus alpinus. J Fish Biol 45:1041-53.
4. Beitinger TL, Bennett WA. 2000. Quantification of the role of acclimation temperature in temperature tolerance of fishes. Environ Biol Fishes 58:277-88.
5. Burggren W. 1982. "Air gulping" improves blood oxygen transport during aquatic hypoxia in the goldfish Carassius auratus. Physiol Zool 55:327-34.
6. Burleson ML, Silva PE. 2011. Cross tolerance to environmental stressors: Effects of hypoxic acclimation on cardiovascular responses of channel catfish (Ictalurus punctatus) to a thermal challenge. J Therm Biol 36:250-4.
7. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Ryu HY, Sbeglia GC, Spagnolo F, Waldron JB, Warsi O, et al. 2013. How does climate change cause extinction? Proc R Soc Lond B Biol Sci 280:1-10.
8. Carveth CJ, Widmer AM, Bonar SA. 2006. Comparison of upper thermal tolerances of native and nonnative fish species in Arizona. Trans Am Fish Soc 135:1433-40.
9. Chown S, Hoffmann A, Kristensen T, Angilletta M, Stenseth N, Pertoldi C. 2010. Adapting to climate change: A perspective from evolutionary physiology. Clim Res 43:3-15.
10. Claireaux G, Lefrançois C. 2007. Linking environmental variability and fish performance: Integration through the concept of scope for activity. Philos Trans R Soc Lond B 362:2031-41.
11. Claireaux G, Webber D. 2000. Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J Sea Res 44:257-65.
12. Claireaux GL, Lagarde J. 1999. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. J Sea Res 42:157-68.
13. Crain CM, Kroeker K, Halpern BS. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304-15.
14. Crocker C, Cech J. 1997. Effects of environmental hypoxia on oxygen consumption rate and swimming activity in juvenile white sturgeon, Acipenser transmontanus, in relation to temperature. Environ Biol Fishes 50:383-9.
15. Darling ES, CôtéIM. 2008. Quantifying the evidence for ecological synergies. Ecol Lett 11:1278-86.
16. Del Toro-Silva FM, Miller JM, Taylor JC, Ellis TA. 2008. Influence of oxygen and temperature on growth and metabolic performance of Paralichthys lethostigma (Pleuronectiformes: Paralichthyidae). J Exp Mar Biol Ecol 358:113-23.
17. Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926-9.
18. DiMichele L, Powers DA. 1982. Physiological basis for swimming endurance differences between LDH-B genotypes of Fundulus heteroclitus. Science 216:1014-6.
19. Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, et al. 2012. Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11-37.
20. Doyle CM, Leberg PL, Klerks PL. 2011. Heritability of heat tolerance in a small livebearing fish, Heterandria formosa. Ecotoxicology 20:535-42.
21. Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP. 2011. Differences in thermal tolerance among sockeye salmon populations. Science 332:109-12.
22. Fangue NA, Hofmeister M, Schulte PM. 2006. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859-72.
23. Fangue NA, Podrabsky JE, Crawshaw LI, Schulte PM. 2009. Countergradient variation in temperature preference in populations of killifish Fundulus heteroclitus. Physiol Biochem Zool 82:776-86.
24. Farrell AP, Richards JG. 2009. Chapter 11-Defining hypoxia: An integrative synthesis of the responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ, editors. Fish physiology. Vol. 27. Oxford: Elsevier Inc. p. 487-503.
25. Faust HA, Gamperl KA, Rodnick KJ. 2004. All rainbow trout (Oncorhynchus mykiss) are not created equal: Intra-Specific variation in cardiac hypoxia tolerance. J Exp Biol 207:1005-15.
26. Ficke AD, Myrick CA, Hansen LJ. 2007. Potential impacts of global climate change on freshwater fisheries. Rev Fish Biol Fisher 17:581-613.
27. Ford T, Beitinger TL. 2005. Temperature tolerance in the goldfish, Carassius auratus. J Therm Biol 30:147-52.
28. Fry F, Hart J. 1948. The relation of temperature to oxygen consumption in the goldfish. Biol Bull 94:66-77.
29. Fry F.E.J. 1971. The effect of environmental factors on the physiology of fish. In: Hoar WS, Randall DJ, editors. Fish physiology. Vol. VI. New York: Academic Press 1-98.
30. Futuyma DJ. 2010. Evolutionary constraint and ecological consequences. Evolution 64:1865-84.
31. Gardiner NM, Munday PL, Nilsson GE. 2010. Counter-Gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PloS One 5:e13299.
32. Healy TM, Schulte PM. 2012. Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85:107-19.
33. Helmuth B, Yamane L, Mach K. 2008. All climate change is local: Understanding and predicting the effects of climate change from an organism's point of view. Stanford J Law Sci Policy 2:18-35.
34. Hochachka PW, Somero GN. 2001. Biochemical adaptation: Mechanism and process in physiological evolution. Oxford: Oxford University Press.
35. Hofmann GE, Todgham AE. 2010. Living in the now: Physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127-45.
36. Holmstrup M, Bindesbøl A-M, Oostingh GJ, Duschl A, Scheil V, Kohler H-R, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, et al. 2010. Interactions between effects of environmental chemicals and natural stressors: A review. Sci Total Environ 408:3746-62.
37. Jourdan-Pineau H, Dupont-Prinet A, Claireaux G, McKenzie DJ. 2010. An investigation of metabolic prioritization in the European sea bass, Dicentrarchus labrax. Physiol Biochem Zool 83:68-77.
38. Killen SS, Marras S, Steffensen JF, McKenzie DJ. 2012. Aerobic capacity influences the spatial position of individuals within fish schools. Proc R Soc Lond B Biol Sci 279:357-64.
39. Klok CJ. 2004. Upper thermal tolerance and oxygen limitation in terrestrial arthropods. J Exp Biol 207:2361-70.
40. Lannig G, Bock C, Sartoris FJ, Portner HO. 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:R902-10.
41. Lefrançois C, Claireaux G. 2003. Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea. Mar Ecol Prog Ser 259:273-84.
42. Mandic M, Todgham AE, Richards JG. 2009. Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc Lond B Biol Sci 276:735-44.
43. Marshall DJ, Dong Y-W, McQuaid CD, Williams GA. 2011. Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. J Exp Biol 214:3649-57.
44. Martinez ML, Chapman LJ, Rees BB. 2009. Population variation in hypoxic responses of the cichlid Psuedocrenilabrus multicolor victoriae. Can J Zool 87:188-94.
45. Meffe GK, Weeks SC, Mulvey M, Kandl KL. 1995. Genetic differences in thermal tolerance of eastern mosquitofish (Gambusia holbrooki) Poeciliidae from ambient and thermal ponds. Can J Fish Aquat Sci 52:2704-11.
46. Mendonça PC, Gamperl AK. 2010. The effects of acute changes in temperature and oxygen availability on cardiac performance in winter flounder (Pseudopleuronectes americanus). Comp Biochem Physiol Part A Mol Integr Physiol 155:245-52.
47. Myers N. 1996. Two key challenges for biodiversity: Discontinuities and synergisms. Biodivers Conserv 5:1025-34.
48. Nilsson GE, Ostlund-Nilsson S, Munday PL. 2010. Effects of elevated temperature on coral reef fishes: Loss of hypoxia tolerance and inability to acclimate. Comp Biochem Physiol Part A Mol Integr Physiol 156:389-93.
49. Overgaard J, Andersen JL, Findsen A, Pedersen PBM, Hansen K, Ozolina K, Wang T. 2012. Aerobic scope and cardiovascular oxygen transport is not compromised at high temperatures in the toad Rhinella marina. J Exp Biol 215:3519-26.
50. Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Ann Rev Ecol Evol System 37:637-69.
51. Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42.
52. Perry GM, Danzmann RG, Ferguson MM, Gibson JP. 2001. Quantitative trait loci for upper thermal tolerance in outbred strains of rainbow trout (Oncorhynchus mykiss). Heredity 86:333-41.
53. Portner H-O. 2001. Climate change and temperature-Dependent biogeography: Oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137-46.
54. Portner H-O. 2005. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From earth history to global change. J Geophys Res 110:1-15.
55. Portner H-O. 2010. Oxygen-And capacity-Limitation of thermal tolerance: A matrix for integrating climate-Related stressor effects in marine ecosystems. J Exp Biol 213:881-93.
56. Portner H-O, Bock C, Knust R, Lannig G, Lucassen M, Mark F, Sartoris F. 2008. Cod and climate in a latitudinal cline: Physiological analyses of climate effects in marine fishes. Clim Res 37:253-70.
57. Portner H-O, Farrell AP. 2008. Physiology and climate change. Science 322:690-2.
58. Portner H-O, Lannig G. 2009. Chapter 4-Oxygen and capacity limited thermal tolerance. In: Richards JG, Farrell AP, Brauner CJ, editors. Fish physiology. Vol. 27. Elsevier. p. 143-91.
59. Portner H-O, Peck MA. 2010. Climate change effects on fishes and fisheries: Towards a cause-And-Effect understanding. J Fish Biol 77:1745-79.
60. Rees BB, Sudradjat FA, Love JW. 2001. Acclimation to hypoxia increases survival time of zebrafish, Danio rerio, during lethal hypoxia. J Exp Zool 289:266-72.
61. Richards JG. 2009. Chapter 10-Metabolic and molecular responses of fish to hypoxia. In: Richards JG, Farrell AP, Brauner CJ, editors. Fish physiology. Vol. 27. Elsevier Inc. p. 443-85.
62. Richards JG, Sardella BA, Schulte PM. 2008. Regulation of pyruvate dehydrogenase in the common killifish, Fundulus heteroclitus, during hypoxia exposure. Am J Physiol Regul Integr Comp Physiol 295:R979-90.
63. Sanderson EW, Jaiteh M, Levy MA, Redford KH, Wannebo AV, Woolmer G. 2002. The human footprint and the last of the wild. BioScience 52:891.
64. Schulte PM, Healy TM, Fangue NA. 2011. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691-702.
65. Schurmann H, Steffensen J. 2006. Lethal oxygen levels at different temperatures and the preferred temperature during hypoxia of the Atlantic cod, Gadus morhua L. J Fish Biol 41:927-34.
66. Secor DH, Gunderson T. 1998. Effects of hypoxia and temperature on survival, growth, and respiration of juvenile Atlantic sturgeon, Acipenser oxyrinchus. Fish Bull 96:603-13.
67. Somero GN. 2002. Thermal physiology and vertical zonation of intertidal animals: Optima, limits, and costs of living. Integr Comp Biol 42:780-9.
68. Somero GN. 2010. The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine "winners" and "losers." J Exp Biol 213:912-20.
69. Somero GN. 2011. Comparative physiology: A "crystal ball" for predicting consequences of global change. Am J Physiol Regul Integr Comp Physiol 301:R1-14.
70. Somorjai I, Danzmann R, Ferguson M. 2003. Distribution of temperature tolerance quantitative trait loci in Arctic charr (Salvelinus alpinus) and inferred homologies in rainbow trout (Oncorhynchus mykiss). Genetics 165:1443-56.
71. Stevens MM, Jackson S, Bester SA, Terblanche JS, Chown SL. 2010. Oxygen limitation and thermal tolerance in two terrestrial arthropod species. J Exp Biol 213:2209-18.
72. Sunday JM, Bates AE, Dulvy NK. 2012. Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686-90.
73. Todgham AE, Schulte PM, Iwama GK. 2005. Cross-Tolerance in the tidepool sculpin: The role of heat shock proteins. Physiol Biochem Zool 78:133-44.
74. Vandeputte M. 2003. Selective breeding of quantitative traits in the common carp (Cyprinus carpio): A review. Aquat Living Resour 16:399-407.
75. Vaquer-Sunyer R, Duarte CM. 2008. Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci USA 105:15452-7.
76. Virani NA, Rees BB. 2000. Oxygen consumption, blood lactate and inter-Individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol Part A Mol Integr Physiol 126:397-405.
77. Visser ME. 2008. Keeping up with a warming world;assessing the rate of adaptation to climate change. Proc R Soc Lond B Biol Sci 275:649-59.
78. White CR, Phillips NF, Seymour RS. 2006. The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125-7.