Niche expansion of the shorthorn sculpin (Myoxocephalus scorpius) to arctic waters is supported by a thermal independence of cardiac performance at low temperature

Canadian Journal of Zoology

Volumn 91, Issue 8, 2013, Pages 573-580

  Farrell, A P ^a   Altimiras, J ^b   Franklin, C E ^c   Axelsson, M ^d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b LINKÖPING UNIVERSITY   (Sweden)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Adrenaline; Cardiac output; Myoxocephalus scorpius; Perfused heart; Power generation; Pressure

Indexed keywords

ACCLIMATION; ADAPTATION; CARDIOVASCULAR SYSTEM; FISH; LOW TEMPERATURE; NICHE; POLAR REGION;

ARCTIC OCEAN;

EID: 84880822876     PISSN: 00084301     EISSN: 14803283     Source Type: Journal    
DOI: 10.1139/cjz-2013-0038     Document Type: Article

References (60)

1. Ask, J.A. 1983. Comparative aspects of adrenergic receptors in the hearts oflower vertebrates. Comp. Biochem. Physiol. PartAPhysiol. 76: 543-552.doi:10.1016/0300-9629(83)90456-5
2. Ask, J.A., Stene-Larsen, G., and Helle, K.B. 1981. Temperature effects on the p2-adrenoceptors of the trout atrium. J. Comp. Physiol. 143:161-168. doi:10.1007/BF00797695.
3. Axelsson, M., Davison, W., Forster, M.E., and Farrell, A.P. 1992. Cardiovascular responses of the red-blooded antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J. Exp. Biol. 167(1): 179-201.PMID:1634863.
4. Axelsson, M. 2005. The circulatory system and its control. In The physiology of polar fishes. Vol. 22. Edited by A.P. Farrell and J.F. Steffensen. Academic Press, New York. pp. 239-280.
5. Axelsson, M., Ehrenstrom, F., and Nilsson, S. 1987. Cholinergic and adrenergic influence on the teleost heart in vivo. Exp. Biol. 46:179-186.PMID:3582588.
6. Brett, J.R. 1971. Energetic responses of salmon to temperature: a study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am. Zool. 11: 99-113.
7. Campbell, H.A., Taylor, E.W., and Egginton, S. 2004. The use of power spectral analysis to determine cardiorespiratory control in the short-horned sculpin Myoxocephalus scorpius. J. Exp. Biol. 207: 1969-1976. doi:10.1242/jeb.00972. PMID:15107449
8. Cech, J.J., Jr., Bridges, D.W., Rowell, D.M., and Balzer, P.J. 1976. Cardiovascular responses of winter flounder, Pseudopleuronectes americanus (Walbaum), to acute temperature increase. Can.J. Zool. 54(8): 1383-1388. doi:10.1139/z76-156. PMID:963643
9. DeVries, A.L., and Steffensen, J.F. 2005. The Arctic and Antarctic polar marine environments. In The physiology of polar fishes. Vol. 22. Edited by A.P. Farrell and J.F. Steffensen. Academic Press, New York and London. pp. 1-22.
10. Eliason, E.J., Clark, T.D., Hague, M.J., Hanson, L.M., Gallagher, Z.S., Jeffries, K.M., Gale, M.K., Patterson, DA., Hinch, S.G., and Farrell, A.P. 2011. Differences in thermal tolerance among sockeye salmon populations. Science, 332(6025): 109-112. doi:10.1126/science.1199158. PMID:21454790.
11. Farrell, A.P. 1997. Effects of temperature on cardiovascular performance. In Global warming implications for freshwater and marine fish. Edited by C.M. Wood and D.G. McDonald. Cambridge University Press, Cambridge. pp. 135-158.
12. Farrell, A.P. 2009. Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J. Exp. Biol. 212: 3771-3780. doi:10.1242/jeb.023671. PMID:19915118.
13. Farrell, A.P., andJones, D.R. 1992. The heart. In Fish physiology. Vol. XII. Edited by W.S. Hoar, D.J. Randall, and A.P. Farrell. Academic Press Inc., San Diego. pp. 1-88.
14. Farrell, A.P., MacLeod, K., and Driedzic, W.R. 1982. The effects of preload, after load, and epinephrine on cardiac performance in the sea raven, Hemitripterus americanus. Can. J. Zool. 60(12): 3165-3171. doi:10.1139/z82-402.
15. Farrell, A.P., MacLeod, K.R., Driedzic, W.R., and Wood, S. 1983. Cardiac performance in the in situ perfused fish heart during extracellular acidosis: interactive effects of adrenaline. J. Exp. Biol. 107: 415-429.PMID:6668460.
16. Farrell, A.P., Hart, T., Wood, S., and Driedzic, W.R. 1984. The effect of extracellular calcium and preload on a teleost heart during extracellular hypercapnic acidosis. Can. J. Zool. 62(7): 1429-1435. doi:10.1139/z84-205.
17. Farrell, A.P., MacLeod, K.R., and Chancey, B. 1986. Intrinsic mechanical properties of the perfused rainbow trout heart and the effects of catecholamines and extracellular calcium under control and acidotic conditions. J. Exp. Biol. 125: 319-345.PMID:3760772.
18. Farrell, A.P., Hammons, A.M., Graham, M.S., and Tibbits, G.F. 1988a. Cardiac growth in rainbow trout, Salmo gairdneri. Can. J. Zool. 66(11): 2368-2373. doi:10.1139/z88-351.
19. Farrell, A.P., Johansen, J.A., and Graham, M.S. 1988b. The role ofthe pericardium in cardiac performance of the trout (Salmo gairdneri). Physiol. Zool. 61: 213-221.
20. Farrell, A.P., Gamperl, A.K., Hicks, J.M.T., Shiels, H.A., and Jain, K.E. 1996. Maximum cardiac performance of rainbow trout (Oncorhynchus mykiss) at temperatures approaching their upper lethal limit. J. Exp. Biol. 199:663-672.PMID: 9318401.
21. Farrell, A.P., Axelsson, M., Altimiras, J., Sandblom, E., and Claireaux, G. 2007. Maximum cardiac performance and adrenergic sensitivity of the sea bass, Dicentrarchus labrax, at high temperatures. J. Exp. Biol. 210: 1216-1224. doi:10.1242/jeb.002881. PMID:17371920.
22. Farrell, A.P., Eliason, E.J., Sandblom, E., and Clark, T.D. 2009. Fish cardiorespiratory physiology in an era of climate change. Can. J. Zool. 87(10): 835-851. doi:10.1139/Z09-092.
23. Franklin, C.E., Davison, W., and Seebacher, F. 2007. Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki. J. Exp. Biol. 210: 3068-3074. doi:10.1242/jeb.003137. PMID:17704081.
24. Fritsche, R. 1990. Effects of hypoxia on blood pressure and heart rate in three marine teleosts. Fish Physiol. Biochem. 8: 85-92. doi:10.1007/BF00004435.
25. Gamperl, A.K., and Farrell, A.P. 2004. Cardiac plasticity in fishes: environmental influences and intraspecific differences. J. Exp. Biol. 207: 2539-2550. doi:10.1242/jeb.01057. PMID:15201287.
26. Gamperl, A.K., Wilkinson, M., and Boutilier, R.G. 1994. p-Adrenoreceptors in the trout (Oncorhynchus mykiss) heart: characterization, quantification, and effects of repeated catecholamine exposure. Gen. Comp. Endocrinol. 95: 259-272. doi:10.1006/gcen.1994.1123. PMID:7958755
27. Goldstein, L., Forster, R.P., and Fanelli, G.M., Jr. 1964. Gill blood flow and ammonia excretion in the marine teleost, Myoxocephalus scorpius. Comp. Biochem. Physiol. 12: 489-499. doi:10.1016/0010-406X(64)90151-3. PMID:14206961.
28. Graham, M.S., and Farrell, A.P. 1989. The effect of temperature acclimation and adrenaline on the performance of a perfused trout heart. Physiol. Zool. 62: 38-61.
29. Hanson, L.M., and Farrell, A.P. 2007. The hypoxic threshold for maximum cardiac performance in rainbow trout Oncorhynchus mykiss (Walbaum) during simulated exercise conditions at 18 °C. J. Fish Biol. 71: 926-932. doi:10.1111/j.1095-8649.2007.01533.x.
30. Hanson, L.M., Ip, Y.K., and Farrell, A.P. 2005. The effect of temperature acclimation on myocardial p-adrenoceptor density and ligand binding affinity in African catfish (Claris gariepinus). Comp. Biochem. Physiol. PartA Mol. Integr. Physiol. 141:164-168. doi:10.1016/j.cbpb.2005.04.018.
31. Hanson, L.M., Obradovich, S., Mouniargi, J., and Farrell, A.P. 2006. The role of adrenergic stimulation in maintaining maximum cardiac performance in rainbow trout (Oncorhynchus mykiss) during hypoxia, hyperkalemia and acidosis at 10 °C. J. Exp. Biol. 209: 2442-2451. doi:10.1242/jeb.02237. PMID: 16788027.
32. Harper, A., Newton, I., and Watt, P. 1995. The effect of temperature on spontaneous action potential discharge of the isolated sinus venosus from winter and summer plaice (Pleuronectes platessa). J. Exp. Biol. 198: 137-140.PMID: 9317498.
33. Hartmund, T., and Gesser, H. 1996. Cardiac force and high-energy phosphates under metabolic inhibition in four ectothermic vertebrates. Am. J. Physiol. 271: R946-R954.PMID:8897986.
34. Imbrogno, S.,Angelone, T.,Adamo, C., Pulera, E., Tota, B., and Cerra, M.C. 2006. p3-Adrenoceptor in the eel (Anguilla anguilla) heart: negative inotropy and NO-cGMP-dependent mechanism. J. Exp. Biol. 209: 4966-4973. doi:10.1242/jeb.02595. PMID:17142685.
35. Joaquim, N., Wagner, G., and Gamperl, A. 2004. Cardiac function and critical swimming speed of the winter flounder (Pleuronectes americanus) at two temperatures. Comp. Biochem. Physiol. PartAMol. Integr. Physiol. 138:277-285. doi:10.1016/j.cbpb.2004.03.016.
36. Keen, J.E., Vianzon, D.-M., Farrell, A.P., and Tibbits, G.F. 1993. Thermal acclimation alters both adrenergic sensitivity and adrenoceptor density in cardiac tissue of rainbow trout. J. Exp. Biol. 181: 27-47.
37. Kiceniuk, J.W., and Jones, D.R. 1977. The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. J. Exp. Biol. 69: 247-260.
38. Lague, S.L., Speers-Roesch, B., Richards, J.G., and Farrell, A.P. 2012. Exceptional cardiac anoxia tolerance in tilapia (Oreochromis hybrid). J. Exp. Biol. 215:1354-1365. doi:10.1242/jeb.063362. PMID:22442374.
39. Lee, C.G., Farrell, A.P., Lotto, A., MacNutt, M.J., Hinch, S.G., and Healey, M.C. 2003. The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho salmon (O. kisutch) salmon stocks. J. Exp. Biol. 206: 3239-3251. doi:10.1242/jeb.00547.
40. Lurman, G.J., Petersen, L.H., and Gamperl, A.K. 2012. In situ cardiac performance of Atlantic cod (Gadus morhua) at cold temperatures: long-term acclimation, acute thermal challenge and the role of adrenaline. J. Exp. Biol 215: 4006-4014. doi:10.1242/jeb.069849.
41. MacCormack, T.J., and Driedzic, W.R. 2004. Cardiorespiratory and tissue adenosine responses to hypoxia and reoxygenation in the short-horned sculpin Myoxocephalus scorpius. J. Exp. Biol. 207: 4157-4164. doi:10.1242/jeb.01251. PMID:15498961.
42. McClelland, G.B., Dalziel, A.C., Fragoso, N.M., and Moyes, C.D. 2005. Muscle remodeling in relation to blood supply: implications for seasonal changes in mitochondrial enzymes. J. Exp. Biol. 208: 515-522. doi:10.1242/jeb.01423. PMID:15671340.
43. Mendonâ, P.C., and Gamperl, A.K. 2009. Nervous and humoral control of cardiac performance in the winter flounder (Pleuronectes americanus) J. Exp. Biol. 212: 934-944. doi:10.1242/jeb.027680.
44. Milligan, C.L., Graham, M.S., and Farrell, A.P. 1989. The response of trout red cells to adrenaline during seasonal acclimation and changes in temperature. J. Fish. Biol. 35: 229-236. doi:10.1111/j.1095-8649.1989.tb02972.x.
45. Nelson, J.A., Tang, Y., and Boutilier, R.G. 1993. Differences in exercise physiology between two Atlantic cod (Gadus morhua) populations from different environments. Physiol. Zool. 67: 330-354.
46. Nelson, J.A., Tang, Y., and Boutilier, R. 1996. The effects of salinity change on the exercise performance oftwo Atlantic cod (Gadus morhua) populations inhabiting different environments. J. Exp. Biol. 199: 1295-1309. PMID:9319167.
47. Pennec, J.P., and Peyraud, C. 1983. Effects of adrenaline on isolated heart of the eel (Anguilla anguilla L.) during winter. Comp. Biochem. Physiol. C, 74: 477-480. PMID:6133696.
48. Randall, D.J. 1970. The circulatory system. In Fish physiology. Vol. 4. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York. pp. 133-172.
49. Randall, D.J., and Perry, S.F. 1992. Catecholamines. In Fish physiology. Vol. 12. Edited by W.S. Hoar and D.J. Randall. Academic Press, NewYork. pp. 255-300.
50. Santer, R.M. 1985. Morphology and innervation of the fish heart. In Advances in anatomy embryology and cell biology. Vol. 89. Springer-Verlag, Berlin. pp. 1-97.
51. Seebacher, F., Davison, W., Lowe, C.J., and Franklin, C.E. 2005. A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes. Biol. Lett. 1: 151-154. doi:10.1098/rsbl.2004.0280. PMID:17148152.
52. 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(5): e62859. doi:10.1371/journal.pone.0062859. PMID: 23690960
53. Shiels, H.A., Vornanen, M., and Farrell, A.P. 2003. Acute temperature change modulates the response of ICa to adrenergic stimulation in fish cardiomyocytes. Physiol. Biochem. Zool. 76: 816-824. doi:10.1086/378918. PMID:14988796.
54. Sidell, B.D., and O'Brien, K.M. 2006. When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes. J. Exp. Biol. 209: 1791-1802. doi:10.1242/jeb.02091. PMID:16651546.
55. 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. doi:10.1242/jeb.004028.PMID:17601961.
56. Sundin, L., Turesson, J., and Taylor, E.W. 2003. Evidence for glutamatergic mechanisms in the vagal sensory pathway initiating cardiorespiratory reflexes in the shorthorn sculpin Myoxocephalus scorpius. J. Exp. Biol. 206: 867-876. doi: 10.1242/jeb.00179. PMID:12547941.
57. Tiitu, V., and Vornanen, M. 2002. Regulation of cardiac contractility in a cold stenothermal fish, the burbot, Lota lota L. J. Exp Biol. 205:1597-1606. PMID: 12000804.
58. Tota, B., Agnisola, C., Schioppa, M., Acierno, R., Harrison, P., and Zummo, G. 1991. Structural and mechanical characteristics of the heart of the icefish, Chionodraco hamatus. In Biology of Antarctic fish. Edited by G. Di Prisco, B. Maresca, and B. Tota. Springer-Verlag, Berlin. pp. 204-219.
59. Wodtke, E., and Cossins, A.R. 1991. Rapid cold-induced changes of membrane order and delta-9-desaturase activity in endoplasmic reticulum of carp liver a time course study of thermal acclimation. Biochim. Biophys. Acta, 1064: 343-350.
60. Zummo, G., Acierno, R., Agnisola, C., and Tota, B. 1995. The heart of the icefish: bioconstruction and adaptation. Brazil J. Med. Biol. Res. 28: 1265-1276.