Thermal onset of cellular and endocrine stress responses correspond to ecological limits in brook trout, an iconic cold-water fish

Conservation Physiology

Volumn 3, Issue 1, 2015, Pages

  Chadwick, Joseph G ^a,b   Nislow, Keith H ^a   McCormick, Stephen D ^a,b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

Author keywords

Climate change; Cortisol; Glucose; Heat shock protein; Salvelinus fontinalis; Temperature

Indexed keywords

EID: 84983605338     PISSN: None     EISSN: 20511434     Source Type: Journal    
DOI: 10.1093/conphys/cov017     Document Type: Article

References (58)

1. Anttila K, Casselman MT, Schulte PM, Farrell AP (2013) Optimum temperature in juvenile salmonids: connecting subcellular indicators of tissue function and whole-organism thermal optimimum. Physiol Biochem Zool 86: 245-256.
2. Baird OE, Krueger CC (2003) Behavioral thermoregulation of brook and rainbow trout: comparison of summer habitat use in an Adirondack River, New York. T Am Fish Soc 132: 1194-1206.
3. Baird OE, Krueger CC, Josephson DC (2006) Growth, movement, and catch of brook, rainbow, and brown trout after stocking into a large, marginally suitable Adirondack river. N Am J Fish Manage 26: 180-189.
4. Baldwin NW (1956) Food consumption and growth of brook trout at different temperatures. T Am Fish Soc 86: 323-328.
5. Basu N, Kennedy CJ, Hodson PV, Iwama GK (2001) Altered stress responses in rainbow trout following a dietary administration of cortisol and beta-napthoflavone. Fish Physiol Biochem 25: 131-140.
6. Biro PA (1998) Staying cool: behavioral thermoregulation during summer by young-of-year brook trout in a lake. T Am Fish Soc 127: 212-222.
7. Boone AN, Ducouret B, Vijayan MM (2002) Glucocorticoid-induced glucose release is abolished in trout hepatocytes with elevated hsp70 content. J Endocrinol 172: R1-R5.
8. Breau C, Cunjak RA, Bremset G (2007) Age-specific aggregation of wild juvenile Atlantic salmon Salmo salar at cool water sources during high temperature events. J Fish Biol 71: 1179-1191.
9. Breau C, Cunjak RA, Peake SJ (2011) Behaviour during elevated water temperatures: can physiology explain movement of juvenile Atlantic salmon to cool water? J Anim Ecol 80: 844-853.
10. Carey JB, McCormick SD (1998) Atlantic salmon smolts are more responsive to an acute handling and confinement stress than parr. Aquaculture 168: 237-253.
11. Currie S, LeBlanc S, Watters MA, Gilmour KM (2010) Agonistic encounters and cellular angst: social interactions induce heat shock proteins in juvenile salmonid fish. Proc Biol Sci 277: 905-913.
12. Curry RA, Brady C, Noakes DLG, Danzmann RG (1997) Use of small streams by young brook trout spawned in a lake. T Am Fish Soc 126: 77-83.
13. Deane EE, Woo NYS (2011) Advances and perspectives on the regulation and expression of piscine heat shock proteins. Rev Fish Biol Fisher 21: 153-185.
14. Dietz TJ, Somero GN (1993) Species-and tissue-specific synthesis patterns for heat-shock proteins HSP70 and HSP90 in several marine teleost fishes. Physiol Zool 66: 863-880.
15. Dubeau SF, Pan F, Tremblay GC, Bradley TM (1998) Thermal shock of salmon in vivo induces the heat shock protein hsp 70 and confers protection against osmotic shock. Aquaculture 168: 311-323.
16. Dwyer WP, Piper RG, Smith CE (1983) Brook trout growth efficiency as affected by temperature. Prog Fish Cult 45: 161-163.
17. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243-282.
18. Feldhaus JW, Heppell SA, Li H, Mesa MG (2010) A physiological approach to quantifying thermal habitat quality for Redband Rainbow Trout (Oncorhynchus mykiss gairdneri) in the south Fork John Day River, Oregon. Environ Biol Fish 87: 277-290.
19. Flebbe PA, Roghair LD, Bruggink JL (2006) Spatial modeling to project southern Appalachian trout distribution in a warmer climate. T Am Fish Soc 135: 1371-1382.
20. Fry FEJ, Hart SA, Walker KF (1946) Lethal temperature relations for a sample of young speckled trout, Salvelinus fontinalis. Univ Toronto Stud Biol Ser 54: 9-35.
21. Gregory TR, Wood CM (1999) The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability, and swimming performance of juvenile rainbow trout. Physiol Biochem Zool 72: 286-295.
22. Hartman KJ, Cox MK (2008) Refinement and testing of a brook trout bioenergetics model. T Am Fish Soc 137: 357-363.
23. Hokanson KE, McCormick JH, Jones BR, Tucker JH (1973) Thermal requirements for maturation, spawning, and embryo survival of brook trout, Salvelinus fontinalis. J Fish Res Board Can 30: 975-984.
24. Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39: 901-909.
25. Kajimura S, Hirano T, Visitacion N, Moriyama S, Aida K, Grau EG (2003) Dual mode of cortisol action on GH/IGF-I/IGF binding proteins in the tilapia, Oreochromis mossambicus. J Endocrinol 178: 91-99.
26. Leal E, Fernández-Durán B, Guillot R, Ríos D, Cerdá-Reverter JM (2011) Stress-induced effects on feeding behavior and growth performance of the sea bass (Dicentrarchus labrax): a self-feeding approach. J Comp Physiol B 181: 1035-1044.
27. Lund SG, Caissie D, Cunjak RA, Vijayan MM, Tufts BL (2002) The effects of environmental heat stress on heat-shock mRNA and protein expression in Miramichi Atlantic salmon (Salmo salar) parr. Can J Fish Aquat Sci 59: 1553-1562.
28. Lund SG, Lund MEA, Tufts BL (2003) Red blood cell Hsp 70 mRNA and protein as bioindicators of temperature stress in the brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60: 460-470.
29. McCormick JH, Jones BR, Hokanson KE (1972) Effects of temperature on growth and survival of young brook trout, Salvelinus fontinalis. J Fish Res Board Can 29: 1107-1112.
30. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50: 656-658.
31. McCormick SD, Shrimpton JM, Carey JB, O'Dea MF, Sloan KE, Moriyama S, Bjornsson BT (1998) Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth factor I and cortisol. Aquaculture 168: 221-235.
32. McMahon TE, Zale AV, Barrows FT, Selong JH, Danehy RJ (2007) Temperature and competition between bull trout and brook trout: a test of the elevation refuge hypothesis. T Am Fish Soc 136: 1313-1326.
33. Meisner JD (1990) Potential loss of thermal habitat for brook trout, due to climatic warming in two southern Ontario streams. T Am Fish Soc 119: 282-291.
34. Meka JM, McCormick SD (2005) Physiological response of wild rainbow trout to angling: impact of angling duration, fish size, body condition, and temperature. Fish Res 72: 311-322.
35. Mesa MG, Weiland LK, Wagner P (2002) Effects of acute thermal stress on the survival, predator avoidance, and physiology of juvenile fall Chinook salmon. Northwest Sci 76: 118-128.
36. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9: 211-268.
37. Pankhurst NW, King HR, Ludke SL (2008a) Relationship between stress, feeding and plasma ghrelin levels in rainbow trout, Oncorhynchus mykiss. Mar Freshw Behav Physiol 41: 53-64.
38. Pankhurst NW, Ludke SL, King HR, Peter RE (2008b) The relationship between acute stress, food intake, endocrine status and life history stage in juvenile farmed Atlantic salmon, Salmo salar. Aquaculture 275: 311-318.
39. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
40. Peterson BC, Small BC (2005) Effects of exogenous cortisol on the GH/IGF-I/IGFBP network in channel catfish. Domest Anim Endocrinol 28: 391-404.
41. Pickering AD (1990) Stress and the suppression of somatic growth in teleost fish. Prog Clin Biol Res 342: 473-479.
42. Pörtner HO (2010) Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213: 881-893.
43. Quigley JT, Hinch SG (2006) Effects of rapid experimental temperature increases on acute physiological stress and behaviour of stream dwelling juvenile Chinook salmon. J Therm Biol 31: 429-441.
44. Rendell JL, Fowler S, Cockshutt A, Currie S (2006) Development-dependent differences in intracellular localization of stress proteins (hsps) in rainbow trout, Oncorhynchus mykiss, following heat shock. Comp Biochem Physiol Part D Genomics Proteomics 1: 238-252.
45. Robinson JM, Josephson DC, Weidel BC, Kraft CE (2010) Influence of variable interannual summer water temperatures on brook trout growth, consumption, reproduction, and mortality in an unstratified Adirondack lake. T Am Fish Soc 139: 685-699.
46. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
47. Smith TR, Tremblay GC, Bradley TM (1999) Characterization of the heat shock protein response of Atlantic salmon (Salmo salar). Fish Physiol Biochem 20: 279-292.
48. Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53: 597-608.
49. Steinhausen MF, Sandblom E, Eliason EJ, Verhille C, Farrell AP (2008) The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka). J Exp Biol 211: 3915-3926.
50. Stitt BC, Burness G, Burgomaster KA, Currie S, McDermid JL, Wilson CC (2014) Intraspecific variation in thermal tolerance and acclimation capacity in brook trout (Salvelinus fontinalis): physiological implications for climate change. Physiol Biochem Zool 87: 15-29.
51. Thorpe JE, Miles MS, Keay DS (1984) Developmental rate, fecundity and egg size in Atlantic salmon, Salmo salar L. Aquaculture 43: 289-305.
52. Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs. J Exp Biol 213: 971-979.
53. Vanderboon J, Vandenthillart GEEJ, Addink ADF (1991) The effects of cortisol administration on intermediary metabolism in teleost fish. Comp Biochem Physiol A Physiol 100: 47-53.
54. Wehrly KE, Wang LZ, Mitro M (2007) Field-based estimates of thermal tolerance limits for trout: incorporating exposure time and temperature fluctuation. T Am Fish Soc 136: 365-374.
55. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77: 591-625.
56. Werner I, Smith TB, Feliciano J, Johnson ML (2005) Heat shock proteins in juvenile steelhead reflect thermal conditions in the Navarro River watershed, California. T Am Fish Soc 134: 399-410.
57. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21: 38-46.
58. Wurtsbaugh WA, Brocksen RW, Goldman CR (1975) Food and distribution of underyearling brook and rainbow trout in Castle Lake, California. T Am Fish Soc 104: 88-95.