Sex-specific differences in cardiac control and hematology of sockeye salmon (Oncorhynchus nerka) approaching their spawning grounds

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 4, 2009, Pages

  Sandblom, Erik ^a,b   Clark, Timothy D ^a   Hinch, Scott G ^a   Farrell, Anthony P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Blood pressure; Cardiac sympathovagal tone; Hematocrit; Hemoglobin; Sex hormones

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; HEMOGLOBIN; HYDROCORTISONE; TESTOSTERONE;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA PRESSURE; ARTICLE; CONTROLLED STUDY; FEMALE; GLOBAL CLIMATE; HEART FUNCTION; HEART RATE; HEMATOCRIT; HEMATOLOGY; MALE; MORTALITY; NONHUMAN; PRIORITY JOURNAL; SEX DETERMINATION; SEXUAL MATURATION; SPAWNING;

ANIMAL MIGRATION; ANIMALS; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; BODY SIZE; ESTRADIOL; FEMALE; HEART; HEART RATE; HEMATOCRIT; HEMODYNAMICS; HEMOGLOBINS; HORMONES; HYDROCORTISONE; MALE; SALMON; SEX FACTORS; SEXUAL BEHAVIOR, ANIMAL; TESTOSTERONE;

EID: 70349627245     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00363.2009     Document Type: Article

References (55)

1. Abdel-Rahman ARA, Merrill RH, Wooles WR. Gender-related differences in the baroreceptor reflex control of heart rate in normotensive humans. J Appl Physiol 77: 606-613, 1994.
2. Altimiras J, Aissaoui A, Tort L, Axesson M. Cholinergic and adrenergic tones in the control of the heart rate in teleosts. How should they be calculated? Comp Biochem Physiol 118A: 131-139, 1997. (Pubitemid 27319806)
3. Altimiras J, Johnstone ADF, Lucas MC, Priede IG. Sex differences in the heart rate variability spectrum of free-swimming Atlantic salmon (Salmo salar L.) during the spawning season. Physiol Biochem Zool 69: 770-784, 1996. (Pubitemid 27006095)
4. Armstrong JD, West CL. Relative ventricular weight of wild Atlantic salmon parr in relation to sex, gonad maturation and migratory activity. J Fish Biol 44: 453-457, 1994.
5. Axelsson M. The circulatory system and its control. In: The Physiology of Polar Fishes, edited by Farrell AP, Steffensen JF. New York: Academic, 2005, p. 239-280.
6. Axelsson M, Davison W, Forster ME, Farrell AP. Cardiovascular responses of the red-blooded Antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J Exp Biol 167: 179-201, 1992.
7. Beacham TD, Lapointe M, Candy JR, McIntosh B, MacConnachie C, Tabata A, Kaukinen K, Deng L, Miller KM, Withler RE. Stock identification of Fraser river Sockeye salmon using microsatellites and major histocompatibility complex variation. Trans Am Fish Soc 133: 1117-1137, 2004. (Pubitemid 39385180)
8. Beacham TD, Lapointe M, Candy JR, Miller KM, Withler RE. DNA in action: rapid application of DNA variation to Sockeye salmon fisheries management. Conserv Genet 5: 411-416, 2004. (Pubitemid 38983088)
9. Burggren WW. Identifying and evaluating patterns in cardiorespiratory physiology. Am Zool 37: 109-115, 1997. (Pubitemid 127754366)
10. Cameron JS. Autonomic nervous tone and regulation of heart rate in the goldfish Carassius auratus. Comp Biochem Physiol 63C: 341-349, 1979.
11. Carruth LL, Dores RM, Maldonado TA, Norris DO, Ruth T, Jones RE. Elevation of plasma cortisol during the spawning migration of landlocked kokanee salmon (Oncorhynchus nerka kennerlyi). Comp Biochem Physiol 127C: 123-131, 2000.
12. Chandler MP, DiCarlo SE. Acute exercise and gender alter cardiac autonomic tonus differently in hypertensive and normotensive rats. Am J Physiol Regul Integr Comp Physiol 274: R510-R516, 1998. (Pubitemid 28103039)
13. Clark RJ, Rodnick KJ. Morphometric and biochemical characteristics of ventricular hypertrophy in male rainbow trout (Oncorhynchus mykiss). J Exp Biol 201: 1541-1552, 1998.
14. Clark RJ, Rodnick KJ. Pressure and volume overloads are associated with ventricular hypertrophy in male rainbow trout. Am J Physiol Regul Integr Comp Physiol 277: R938-R946, 1999.
15. Clark TD, Eliason EJ, Sandblom E, Hinch SG, Farrell AP. Calibration of a hand-held haemoglobin analyser for use on fish blood. J Fish Biol 73: 2587-2595, 2008.
16. Clark TD, Hinch SG, Taylor BD, Frappell PB, Farrell AP. Sex differences in circulatory oxygen transport parameters of sockeye salmon (Oncorhynchus nerka) on the spawning ground. J Comp Physiol 179B: 663-671, 2009.
17. Clark TD, Sandblom E, Cox GK, Hinch SG, Farrell AP. Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha). Am J Physiol Regul Integr Comp Physiol 295: R1631-R1639, 2008.
18. Clark TD, Taylor BD, Seymour RS, Ellis D, Buchanan J, Fitzgibbon QP, Frappell PB. Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna. Proc Biol Sci 275: 2841-2850, 2008. (Pubitemid 352790144)
19. Convertino VA. Gender differences in autonomic functions associated with blood pressure regulation. Am J Physiol Regul Integr Comp Physiol 275: R1909-R1920, 1998. (Pubitemid 128731921)
20. Cotter PA, Han AJ, Everson JJ, Rodnick KJ. Cardiac hemodynamics of the rainbow trout (Oncorhynchus mykiss) using simultaneous Doppler echocardiography and electrocardiography. J Exp Zool A Ecol Genet Physiol 309: 243-254, 2008.
21. Crossin GT, Hinch SG, Cooke SJ, Welch DW, Patterson DA, Jones SRM, Lotto AG, Leggatt RA, Mathes MT, Shrimpton JM, Van der Kraak G, Farrell AP. Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration. Can J Zool 86: 127-140, 2008.
22. Dart AM, Du XJ, Kingwell BA. Gender, sex hormones and autonomic nervous control of the cardiovascular system. Cardiovasc Res 53: 678-687, 2002. (Pubitemid 34175261)
23. Davie PS, Thorarensen H. Heart growth in rainbow trout in response to exogenous testosterone and 17-α methyltestosterone. Comp Biochem Physiol 117A: 227-230, 1997. (Pubitemid 27243538)
24. Dingle H. Migration: the Biology of Life on the Move. Oxford: Oxford University Press, 1996.
25. Farrar RS, Rodnick KJ. Sex-dependent effects of gonadal steroids and cortisol on cardiac contractility in rainbow trout. J Exp Biol 207: 2083-2093, 2004.
26. Farrell AP. Cardiovascular responses in the sea raven, Hemitripterus americanus, elicited by vascular compression. J Exp Biol 122: 65-80, 1986.
27. Farrell AP, Jones DR. The heart. In: Fish Physiology, The Cardiovascular System, edited by Hoar WS, Randal DJ, and Farrell AP. New York: Academic, 1992, p. 1-88.
28. Farrell AP, MacLeod KR, Scott C. Cardiac performance of the trout (Salmo gairdneri) heart during acidosis: effects of low bicarbonate, lactate and cortisol. Comp Biochem Physiol 91A: 271-277, 1988. (Pubitemid 18236142)
29. Farrell AP, Simonot DL, Seymour RS, Clark TD. A novel technique for estimating the compact myocardium in fishes reveals surprising results for an athletic air-breathing fish, the Pacific tarpon. J Fish Biol 71: 389-398, 2007.
30. Faust HA, Gamperl AK, Rodnick KJ. All rainbow trout (Oncorhynchus mykiss) are not created equal: intra-specific variation in cardiac hypoxia tolerance. J Exp Biol 207: 1005-1015, 2004.
31. Fent K. Effects of organotin compounds in fish: from the molecular to the population level. In: Fish Ecotoxicology, edited by Braunbeck T, Hinton DE, and Streit B. Berlin: Birkhäuser, 1998, p. 259-302.
32. Franklin CE, Davie PS. Sexual maturity can double heart mass and cardiac power output in male rainbow trout. J Exp Biol 171: 139-148, 1992.
33. Gamperl AK, Farrell AP. Cardiac plasticity in fishes: environmental influences and intraspecific differences. J Exp Biol 207: 2539-2550, 2004.
34. Hanson KC, Gravel MA, Graham A, Shoji A, Cooke SJ. Sexual variation in fisheries research and management: when does sex matter? Rev Fish Sci 16: 421-436, 2008.
35. Holeton GF, Randall DJ. Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46: 297-305, 1967.
36. Hruska KA, Hinch SG, Healey MC, Farrell AP. Electromyogram telemetry, nondestructive physiological biopsy, and genetic markers: linking recent techniques with behavioral observations for the study of reproductive success in sockeye salmon mating systems. Am Fish Soc Symp 54: 17-29, 2007.
37. Kakizawa S, Kaneko T, Ogasawara T, Hirano T. Changes in plasma somatolactin levels during spawning migration of chum salmon (Oncorhynchus keta). Fish Physiol Biochem 14: 93-101, 1995.
38. Keen JE, Aota S, Brill RW, Farrell AP, Randall DJ. Cholinergic and adrenergic regulation of heart rate and ventral aortic pressure in two species of tropical tunas, Katsuwonus pelamis and Thunnus albacares. Can J Zool 73: 1681-1688, 1995.
39. Kubokawa K, Watanabe T, Yoshioka M, Iwata M. Effects of acute stress on plasma cortisol, sex steroid hormone and glucose levels in male and female sockeye salmon during the breeding season. Aquaculture 172: 335, 1999. (Pubitemid 29103003)
40. Leatherland JF, Down NE, Donaldson EM, Dye HM. Changes in plasma thyroid hormone levels in pink salmon, Oncorhynchus gorbuscha, during their spawning migration in the Fraser River (Canada). J Fish Biol 35: 199-205, 1989.
41. Lucas MC, Johnstone ADF, Priede IG. Use of physiological telemetry as a method of estimating metabolism of fish in the natural environment. Trans Am Fish Soc 122: 822-833, 1993.
42. Luk'yanenko VI, Raspopov VM. Sexual dimorphism and seasonal dynamics of the morphological parameters of the Russian sturgeon in the river period of life. In: Tez Otchetn sessii Tsentr n.-i. in-ta osetrovogo kh-va. Astrakhan, Russia: Central Sturgeon Fisheries Research Institute, 1972.
43. Nilsson S. Autonomic Nerve Function in the Vertebrates. Berlin: Springer, 1983.
44. Pavlidis M, Dimitriou D, Dessypris A. Testosterone and 17β-estradiol plasma fluctuations throughout spawning period in male and female rainbow trout, Oncorhynchus mykiss (Walbaum), kept under several photoperiod regimes. Ann Zool Fenn 31: 319-327, 1994. (Pubitemid 2159218)
45. Pörtner HO, Farrell AP. Physiology and climate change. Science 322: 690-692, 2008.
46. Randall DJ. The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100: 275-288, 1982.
47. Randall DJ, Smith JC. The regulation of cardiac activity in fish in a hypoxia environment. Physiol Zool 40: 104-113, 1967.
48. Sandblom E, Axelsson M. Baroreflex mediated control of heart rate and vascular capacitance in trout. J Exp Biol 208: 821-829, 2005. (Pubitemid 40428159)
49. Santer RM. Ultrastructural and histochemical studies on the innervation of the heart of a teleost, Pleuronectes platessa L. Z Zellforsch Mikrosk Anat 131: 519-528, 1972.
50. Schmidt PJ, Idler DR. Steroid hormones in the plasma of salmon at various states of maturation. Gen Comp Endocrinol 2: 204-214, 1962.
51. Soivio A, Nynolm K, Westman K. A technique for repeated sampling of the blood of individual resting fish. J Exp Biol 63: 207-217, 1975.
52. Sower SA, Schreck CB. Steroid and thyroid hormones during sexual maturation of coho salmon (Oncorhynchus kisutch) in seawater or fresh water. Gen Comp Endocrinol 47: 42-53, 1982.
53. Steinhausen MF, Sandblom E, Eliason E, Verhille C, Farrell AP. The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka). J Exp Biol 211: 3915-3926, 2008.
54. Thorarensen H, Knight C, Davie PS. Seasonal changes in 11-ketotestosterone and relative ventricle mass in wild rainbow trout, Oncorhynchus mykiss. N Z J Mar Freshwater Res 30: 397-402, 1996. (Pubitemid 26369326)
55. Thorarensen H, Young G, Davie PS. 11-Ketotestosterone stimulates growth of heart and red muscle in rainbow trout. Can J Zool 74: 912-917, 1996. (Pubitemid 126509917)