Abstract
Catecholamines increase arterial pressure by increasing cardiac output (Q) and stroke volume (V s), while angiotensin II (ang II) also increases vascular resistance (R sys) in the Antarctic fish Pagothenia borchgrevinki. Adrenaline, phenylephrine and ang II (Asn1, Val5) were injected into P. borchgrevinki. Cardiovascular variables, including central venous pressure (P cv) and mean circulatory filling pressure (P mcf; an index of venous capacitance), were recorded to investigate if venous vasoconstriction can explain the increased V s and Q and the arterial pressor response in this species. Routine P cv and P mcf were 0.11 ± 0.01 and 0.18 ± 0.02 kPa, respectively. All of the drugs caused moderate increases in P cv and P mcf and the responses were attenuated after α-adrenergic blockade with prazosin. Although dorsal aortic pressure (P da) also increased in response to all agonists, the mechanisms differed. Adrenaline caused sustained increases in V s and Q, while R sys only rose transiently. Ang II had a slower effect than adrenaline and increased both R sys and Q, while phenylephrine only increased R sys. This study demonstrates that P cv is positive and controlled by an α-adrenergic mechanism in P. borchgrevinki. However, given the relatively small venous response to adrenaline it seems more likely that the increases in V s and Q from this agonist are due to direct effects on the heart.
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Agnisola C, Acierno R, Calvo J, Farina F, Tota B (1997) In vitro cardiac performance in the sub-antarctic notothenioids Eleginops maclovinus (Subfamily Eleginopinae), Paranothothenia magellanica, and Patagonotothen Tessellata (Subfamily Nototheniinae). Comp Biochem Physiol A 118:1437–1445
Axelsson M, Agnisola C, Nilsson S, Tota B (1996) Fish cardio-circulatory function in the cold. In: Pörtner HO, Playle RC (eds) Cold ocean physiology. Cambridge University Press, Cambridge
Axelsson M (2005) The circulatory system and its control. In: Farrell AP, Steffensen JF (eds) The physiology of polar fishes, vol 22. Academic Press, Dublin, pp 239–280
Axelsson M, Davison B, Forster M, Nilsson S (1994) Blood pressure control in the Antarctic fish Pagothenia borchgrevinki. J Exp Biol 190:265–279
Axelsson M, Davison W, Forster ME, Farrell AP (1992) Cardiovascular responses of the red-blooded Antarctic fishes Pagothenia bernacchii and P. borchgrevinki. J Exp Biol 167:179–201
Axelsson M, Thorarensen H, Nilsson S, Farrell AP (2000) Gastrointestinal blood flow in the red Irish lord, Hemilepidotus hemilepidotus: long-term effects of feeding and adrenergic control. J Comp Physiol 170:145–152
Bernier NJ, McKendry JE, Perry SF (1999) Blood pressure regulation during hypotension in two teleost species: Differential involvement of the renin-angiotensin and adrenergic systems. J Exp Biol 202:1677–1690
Bernier NJ, Perry SF (1999) Cardiovascular effects of angiotensin-II- mediated adrenaline release in rainbow trout Oncorhynchus mykiss. J Exp Biol 202:55–66
Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:212–220
Davison W, Axelsson M, Forster M, Nilsson S (1995) Cardiovascular responses to acute handling stress in the Antarctic fish Trematomus bernacchii are not mediated by circulatory catecholamines. Fish Physiol Biochem 14:253–257
Davison W, Axelsson M, Nilsson S, Forster ME (1997) Cardiovascular control in antarctic notothenioid fishes. Comp Biochem Physiol A 118:1001–1008
Davison W, Franklin CE (2003) Hypertension in Pagothenia borchgrevinki caused by X-cell disease. J Fish Biol 63:129–136
De Vries AL, Steffensen JF (2005) The Arctic and Antarctic polar marine environments. In: Farrell AP, Steffensen JF (eds) The physiology of polar fishes, vol 22. Academic Press, pp 1–24
Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107
Egginton S (1994) Stress response in two Antarctic teleosts (Notothenia coriiceps Richardson and Chaenocephalus aceratus Lonnberg) following capture and surgery. J Comp Physiol B 164(6):482–491
Egginton S, Campbell H, Davison W (2006) Cardiovascular control in Antarctic fish. Deep Sea Res Part II Top Stud Oceanogr 53:1115–1130
Farrell AP (1991) From hagfish to tuna: a perspective on cardiac function in fish. Physiol Zool 64:1137–1164
Farrell AP, Jones DR (1992) The heart. In: Hoar WS, Randal DJ, Farrell AP (eds) Fish physiology, the cardiovascular system, vol XII. Academic Press Inc, MA, pp 1–88
Forster ME, Davison W, Axelsson M, Sundin L, Franklin CE, Gieseg S (1998) Catecholamine release in heat-stressed Antarctic fish causes proton extrusion by the red cells. J Comp Physiol B 168:345–352
Franklin CE, Davison W (1988) X-cells in the gills of an Antarctic teleost, Pagothenia borchgrevinki. J Fish Biol 32:341–353
Hunt BM, Hoefling K, Cheng CHC (2003) Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarct Sci 15:333–338
Macdonald JA, Montgomery JC, Wells RMG (1987) Comparative physiology of Antarctic fishes. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology, vol 24. Academic Press, London, pp 321–388
Minerick AR, Chang HC, Hoagland TM, Olson KR (2003) Dynamic synchronization analysis of venous pressure-driven cardiac output in rainbow trout. Am J Physiol 285:R889–R896
Olson K, Chavez A, Conklin D, Cousins K, Farrell A, Ferlic R, Keen J, Kne T, Kowalski K, Veldman T (1994) Localization of angiotensin II responses in the trout cardiovascular system. J Exp Biol 194:117–138
Olson KR (1992) Blood and extracellular fluid volume regulation: role of the renin angiotensin system, kallikrein-kinin system, and atrial natriuretic peptides. In: Randall DJ, Hoar WS, Farrell AP (eds) Fish physiology, vol XIIB. Academic Press, San Diego, pp 135–254
Olson KR, Farrell AP (2006) The cardiovascular system. In: Evans DH, Claiborne JB (eds) The physiology of fishes. Taylor and Francis, London
Oudit GY, Butler DG (1995) Angiotensin II and cardiovascular regulation in a freshwater teleost, Anguilla rostrata LeSueur. Am J Physiol 269:R726–R735
Pang CC (2001) Autonomic control of the venous system in health and disease: effects of drugs. Pharmacol Ther 90:179–230
Rothe CF (1984) Control of capacitance vessels. In: Shepherd AP, Granger DN (eds) Physiology of the intestinal circulation. Raven Press, New York, pp 73–81
Sandblom E, Axelsson M (2005) Baroreflex mediated control of heart rate and vascular capacitance in trout. J Exp Biol 208:821–829
Sandblom E, Axelsson M (2006) Adrenergic control of venous capacitance during moderate hypoxia in the rainbow trout (Oncorhynchus mykiss): role of neural and circulating catecholamines. Am J Physiol 291:R711–R718
Sandblom E, Axelsson M (2007a) The venous circulation: A piscine perspective. Comp Biochem Physiol A 148:785–801
Sandblom E, Axelsson M (2007b) Venous hemodynamic responses to acute temperature increase in the rainbow trout (Oncorhynchus mykiss). Am J Physiol 292:R2292–R2298
Sandblom E, Farrell AP, Altimiras J, Axelsson M, Claireaux G (2005) Cardiac preload and venous return in swimming sea bass (Dicentrarchus labrax L.). J Exp Biol 208:1927–1935
Sandblom E, Axelsson M, Farrell AP (2006a) Central venous pressure and mean circulatory filling pressure in the dogfish Squalus acanthias: adrenergic control and role of the pericardium. Am J Physiol 291:R1465–R1473
Sandblom E, Axelsson M, McKenzie DJ (2006b) Venous responses during exercise in rainbow trout, Oncorhynchus mykiss: α-adrenergic control and the antihypotensive function of the renin-angiotensin system. Comp Biochem Physiol A 144:401–409
Sandblom E, Axelsson M and Davison W (2008) Enforced exercise, but not acute temperature elevation, decreases venous capacitance in the stenothermal Antarctic fish Pagothenia borchgrevinki. J Comp Physiol B, 178(7):845–851
Skals M, Skovgaard N, Taylor EW, Leite CA, Abe AS, Wang T (2006) Cardiovascular changes under normoxic and hypoxic conditions in the air-breathing teleost Synbranchus marmoratus: importance of the venous system. J Exp Biol 209:4167–4173
Sundin L, Davison W, Forster M, Axelsson M (1998) A role of 5-HT2 receptors in the gill vasculature of the antarctic fish Pagothenia borchgrevinki. J Exp Biol 201:2129–2138
Sundin L, Axelsson M, Davison W, Forster ME (1999) Cardiovascular responses to adenosine in the antarctic fish Pagothenia borchgrevinki. J Exp Biol 202:2259–2267
Tota B, Acierno R, Agnisola C (1991) Mechanical performance of the isolated and perfused heart of the hemoglobinless Antarctic icefish Chionodraco hamatus (Lönnberg): effects of loading conditions and temperature. Phil Trans B 332:191–198
Uva BM, Masini MA, Devecchi M, Napoli L (1991) Renin-angiotensin system in antarctic fishes. Comp Biochem Physiol 100A:897–900
Whiteley NM, Egginton S (1999) Antarctic fishes have a limited capacity for catecholamine synthesis. J Exp Biol 202:3623–3629
Wood CM, Shelton G (1980) Cardiovascular dynamics and adrenergic responses of the rainbow trout in vivo. J Exp Biol 87:247–270
Zhang Y, Weaver L Jr, Ibeawuchi A, Olson KR (1998) Catecholaminergic regulation of venous function in the rainbow trout. Am J Physiol 274:R1195–R1202
Acknowledgments
The authors would like to thank Antarctica New Zealand and base staff of Scott Base for logistics support and the ability to visit and work in Antarctica. M. A. was financially supported by research grants from the Swedish research council and E. S. was supported by a travel grant from the Swedish research council.
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Communicated by G. Heldmaier.
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Sandblom, E., Axelsson, M. & Davison, W. Circulatory function at sub-zero temperature: venous responses to catecholamines and angiotensin II in the Antarctic fish Pagothenia borchgrevinki . J Comp Physiol B 179, 165–173 (2009). https://doi.org/10.1007/s00360-008-0299-z
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DOI: https://doi.org/10.1007/s00360-008-0299-z