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Journal of Comparative Physiology B

, Volume 183, Issue 6, pp 801–809 | Cite as

Cardiac performance correlates of relative heart ventricle mass in amphibians

  • Gregory J. Kluthe
  • Stanley S. HillmanEmail author
Original Paper

Abstract

This study used an in situ heart preparation to analyze the power output and stroke work of spontaneously beating hearts of four anurans (Rhinella marina, Lithobates catesbeianus, Xenopus laevis, Pyxicephalus edulis) and three urodeles (Necturus maculosus, Ambystoma tigrinum, Amphiuma tridactylum) that span a representative range of relative ventricle mass (RVM) found in amphibians. Previous research has documented that RVM correlates with dehydration tolerance and maximal aerobic capacity in amphibians. The power output (mW g−1 ventricle mass) and stroke work (mJ g−1 ventricle muscle mass) were independent of RVM and were indistinguishable from previously published results for fish and reptiles. RVM was significantly correlated with maximum power output (P max, mW kg−1 body mass), stroke volume, cardiac output, afterload pressure (P O) at P max, and preload pressure (P I) at P max. P I at P max and P O at P max also correlated very closely with each other. The increases in both P I and P O at maximal power outputs in large hearts suggest that concomitant increases in blood volume and/or increased modulation of vascular compliance either anatomically or via sympathetic tone on the venous vasculature would be necessary to achieve P max in vivo. Hypotheses for variation in RVM and its concomitant increased P max in amphibians are developed.

Keywords

Ventricle mass Cardiac power output Amphibians 

Notes

Acknowledgments

Financial assistance was provided by National Science Foundation IOS-0843082 (SH) and the Forbes-Lea Fund (GK). The work represents parts of an MS Thesis submitted to PSU. The guidance and input received from committee members Drs. Gary Brodowicz, and Jason Podrabsky is greatly appreciated. We thank the anonymous reviewers for their thoughtful input.

References

  1. Acierno R, Gattuso A, Cerra MC, Pellegrino D, Agnisola C, Tota B (1994) The isolated and perfused working heart of the frog, Rana esculenta: an improved preparation. Gen Pharmacol 25:521–526PubMedCrossRefGoogle Scholar
  2. Acierno R, Agnisola C, Tota B, Sidell BD (1997) Myoglobin enhances cardiac performance in Antarctic icefish species that express the protein. Am J Physiol 273:R100–R106PubMedGoogle Scholar
  3. Agnisola C, Venzi R, Houlihan DF, Tota B (1994) Coronary flow-pressure relationship in the working isolated fish heart: trout (Oncorhynchus mykiss) versus torpedo (Torpedo marmorata). Philos Trans R Soc B 343:189–198CrossRefGoogle Scholar
  4. Agnisola C, Acierno R, Calvo J, Farina F, Tota B (1997) In vitro cardiac performance in the sub-Antarctic notothenioids Eleginops maclovinus (subfamily Eleginopinae), Paranotothenia magellanica, and Patagonotothen tessellata (subfamily Nototheniinae). Comp Biochem Physiol A 118:1437–1445CrossRefGoogle Scholar
  5. Allaby M (1994) Oxford concise dictionary of ecology. Oxford University Press, New YorkGoogle Scholar
  6. Axelsson M, Wahlqvist I, Ehrenstrom F (1989) Cardiovascular regulation in the mudpuppy, Necturus maculosus at rest and during short-term exercise. Exp Biol 48:253–259PubMedGoogle Scholar
  7. Blakemore C, Cuthbert A, Jennett S, Porter R, Schiebinger L, Sears T, Tansey T (2001) The Oxford companion to the body. Oxford University Press, OxfordGoogle Scholar
  8. Blank JM, Morrissette JM, Davie PS, Block BA (2002) Effects of temperature, epinephrine and Ca2+ on the hearts of yellowfin tuna (Thunnus albacares). J Exp Biol 205:1881–1888PubMedGoogle Scholar
  9. Blank JM, Morrissette JM, Landeira-Fernandez AM, Blackwell SB, Williams TD, Block BA (2004) In situ cardiac performance of Pacific bluefin tuna hearts in response to acute temperature change. J Exp Biol 207:881–890PubMedCrossRefGoogle Scholar
  10. Conklin D, Chavas A, Duff WD, Weaver Jr L, Zhang Y, KR O (1997) Cardiovascular effects of arginine vasotocin in the rainbow trout Oncorhynchus mykiss. J Exp Biol 200:2812–2832Google Scholar
  11. Davidson DW, Davie PS (2001) Mechanical efficiency of isolated in situ perfused hearts of the eel Anguilla australis. Comp Biochem Physiol A 128:167–175CrossRefGoogle Scholar
  12. Davie PS, Farrell AP (1991) Cardiac performance of an isolated heart preparation from the dogfish: the effects of hypoxia and coronary artery perfusion. Can J Zool 69:1822–1828CrossRefGoogle Scholar
  13. Davie PS, Farrell AP (2005) Cardiac performance of an isolated eel heart: effects of hypoxia and responses to coronary artery occlusion. J Exp Zool 262:113–121CrossRefGoogle Scholar
  14. Farrell AP (1991) From hagfish to tuna: a perspective on cardiac function in fish. Physiol Zool 64:1137–1164Google Scholar
  15. Farrell AP, Stecyk JA (2007) The heart as a working model to explore themes and strategies for anoxic survival in ectothermic vertebrates. Comp Biochem Physiol A 147:300–312CrossRefGoogle Scholar
  16. Farrell AP, MacLeod KR, Driedzic WR, Wood S (1983) Cardiac performance in the in situ perfused fish heart during extracellular acidosis: interactive effects of adrenaline. J Exp Biol 107:415–429PubMedGoogle Scholar
  17. Farrell AP, Wood S, Hart T (1985) Myocardial oxygen consumption in the sea raven Hemitripterus americanus the effect of volume loading, pressure loading, and progressive hypoxia. J Exp Biol 117:237–250Google Scholar
  18. Farrell AP, Davie PS, Franklin CE, Johansen JA, Brill RB (1992) Cardiac physiology in tunas: I. In vitro perfused heart preparation from yellowfin and skipjack tunas. Can J Zool 70:1200–1210CrossRefGoogle Scholar
  19. Feng HZ, Chen X, Hossain MM, Jin JP (2012) Toad heart utilizes exclusively slow skeletal muscle troponin T: an evolutionary adaptation with potential functional benefits. J Biol Chem 287:29753–29764PubMedCrossRefGoogle Scholar
  20. Forster ME (1989) Performance of the heart of the hagfish, Eptatretus cirrhatus. Fish Physiol Biochem 6:327–331CrossRefGoogle Scholar
  21. Franklin CE (1994) Intrinsic properties of an in situ turtle heart (Emydura signata) preparation perfused via both atria. Comp Biochem Physiol A 107:501–507CrossRefGoogle Scholar
  22. Franklin CE, Axelsson M (1994) The intrinsic properties of an in situ perfused crocodile heart. J Exp Biol 186:269–288PubMedGoogle Scholar
  23. Garofalo F, Imbrogno S, Gattuso A, Spena A, Cerra MC (2006) Cardiac morpho-dynamics in Rana esculenta: influence of sex and season. Comp Biochem Physiol 145A:82–89Google Scholar
  24. Gatten RE, Miller K, Full RJ (1992) Energetics at rest and during locomotion. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press, Chicago, pp 314–377Google Scholar
  25. Graham MS, Farrell AP (1989) The effect of temperature acclimation and adrenaline on the performance of a perfused trout heart. Physiol Zool 62:38–61Google Scholar
  26. Graham JB, Lee HJ (2004) Breathing air in air: in what ways might extant amphibious fish biology relate to prevailing concepts about early tetrapods, the evolution of air breathing, and the vertebrate land transition? Physiol Biochem Zool 77:720–731PubMedCrossRefGoogle Scholar
  27. Hedrick MS, Palioca WB, Hillman SS (1999) Effects of temperature and physical activity on blood flow shunts and intracardiac mixing in the toad Bufo marinus. Physiol Biochem Zool 72:509–519Google Scholar
  28. Hillman SS (1976) Cardiovascular correlates of maximal oxygen consumption rates in anuran amphibians. J Comp Physiol B 109:199–207CrossRefGoogle Scholar
  29. Hillman SS (1980) Physiological correlates of differential dehydration tolerance in anuran amphibians. Copeia 1980:125–129CrossRefGoogle Scholar
  30. Hillman SS (1984) Inotropic influence of dehydration and hyperosmolal solutions on amphibian cardiac muscle. J Comp Physiol 154B:325–328Google Scholar
  31. Hillman SS, Withers PC, Hedrick MS, Kimmel PB (1985) The effects of erythrocythemia on blood viscosity, maximal systemic oxygen transport capacity and maximal rates of oxygen consumption in an amphibian. J Comp Physiol 155B:577–581Google Scholar
  32. Hillman SS, Withers P, Kimmel PB (1998) Plasma catecholamines with hemorrhage in the bullfrog, Rana catesbeiana. J Exp Zool 280:174–181PubMedCrossRefGoogle Scholar
  33. Hillman SS, Withers PC, Drewes RC (2000) Correlation of ventricle mass and dehydration tolerance in amphibians. Herpetologica 56:413–420Google Scholar
  34. Hillman SS, Withers PC, Drewes RC, Hillyard SD (2009) Ecological and environmental physiology of amphibians. Oxford University Press, OxfordGoogle Scholar
  35. Hillman SS, DeGrauw EA, Hoagland T, Hancock T, Withers P (2010) The role of vascular and interstitial compliance and vascular volume in the regulation of blood volume in two species of anuran. Physiol Biochem Zool 83:55–67PubMedCrossRefGoogle Scholar
  36. Hillman SS, Hancock T, Hedrick MS (2013) A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange. J Comp Physiol B 183:167–179PubMedCrossRefGoogle Scholar
  37. Hoagland TM, Weaver L, Conlon MJ, Wang Y, Olsen KR (2000) Effects of endothelin-1 and homologous trout endothelin on cardiovascular function in rainbow trout. Am J Physiol 278(2):460–468Google Scholar
  38. Hoyt RW, Eldridge M, Wood SC (1984) Noninvasive pulsed Doppler determination of cardiac output in an unanesthetized neotenic salamander, Ambystoma tigrinum. J Exp Zool 230:491–493CrossRefGoogle Scholar
  39. Johansen K (1963) Cardiovascular dynamics in the amphibian, Amphiuma tridactylum. Acta Physiol Scand Suppl 217:1–82Google Scholar
  40. Johnston IA, Fitch N, Zummo G, Wood RE, Harrison P, Tota B (1983) Morphometric and ultrastructural features of the ventricular myocardium of the haemoglobin-less icefish Chaenocephalus aceratus. Comp Biochem Physiol A 76:475–480CrossRefGoogle Scholar
  41. McKean T, Scherzer A, Park A (1997) Hypoxia and ischaemia in buffer-perfused toad hearts. J Exp Biol 200:2575–2581PubMedGoogle Scholar
  42. Mendonca PC, Genge AG, Deitch EJ, Gamperl AK (2007) Mechanisms responsible for the enhanced pumping capacity of the in situ winter flounder heart (Pseudopleuronectes americanus). Am J Physiol 293:R1112–R1120CrossRefGoogle Scholar
  43. Olson KR, Farrell AP (2006) The cardiovascular system, chap 4. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. Taylor and Francis Group, Boca RatonGoogle Scholar
  44. Olson KR, Conklin DJ, Weaver L (1997) Cardiovascular effects of homologous bradykinin in rainbow trout. Am J Physiol 272:R1112–R1120PubMedGoogle Scholar
  45. Ostadal B (1979) Developmental relationships between structure, blood supply and metabolic patterns of the vertebrate heart. Cor Vasa 20:380–386Google Scholar
  46. Pough FH (1980) The advantages of ectothermy for tetrapods. Am Nat 115:95–112CrossRefGoogle Scholar
  47. Poupa O, Lindstrom L (1983) Comparative and scaling aspects of heart and body weights with reference to blood supply of cardiac fibers. Comp Biochem Physiol 76A:413–421CrossRefGoogle Scholar
  48. Poupa O, Ostadahl B (1969) Experimental cardiomegalies and “cardiomegalies” in free-living animals. Ann N Y Acad Sci 156:445–468PubMedCrossRefGoogle Scholar
  49. Romero SMB, Pereira AF, Garofalo MAR, Hoffman A (2004) Effects of exercise on plasma catecholamine levels in the toad, Bufo paracnemis: role of the adrenals and neural control. J Exp Zool 301A:911–918CrossRefGoogle Scholar
  50. Sandblom E, Axelsson M, Farrell AP (2006) Central venous pressure and mean circulatory filling pressure in the dogfish, Squalus acanthias: adrenergic control and the role of the pericardium. Am J Physiol 291:R1465–R1473Google Scholar
  51. Santer RM, Walker MG, Emerson L, Witthames PR (1983) On the morphology of the heart ventricle in marine teleost fish (Teleostei). Comp Biochem Physiol 76A:453–457CrossRefGoogle Scholar
  52. Schmidt-Nielsen K (1972) Locomotion: energy cost of swimming, flying, and running. Science 177:222–228PubMedCrossRefGoogle Scholar
  53. Titu V, Vornamen M (2005) Morphology and fine structure of the heart of the burbot, a cold stenothermal fish. J Fish Biol 61:106–121CrossRefGoogle Scholar
  54. Tota B, Acierno R, Agnisola C (1991) Mechanical performance of the isolated and perfused heart of the haemoglobinless Antarctic icefish Chionodraco hamatus: effects of loading conditions and temperature. Philos Trans R Soc B 332:191–198CrossRefGoogle Scholar
  55. Tota B, Cerra CC, Gattuso A (2010) Catecholamines, cardiac natriuretic peptides and chromogranin A: evolution and physiopathology of a “whip-brake” system of the endocrine heart. J Exp Biol 213:3081–3103PubMedCrossRefGoogle Scholar
  56. West NH, Smits AW (1994) Cardiac output in conscious toads (Bufo marinus). J Exp Biol 186:315–323PubMedGoogle Scholar
  57. Withers PC, Hillman SS (1988) A steady-state model of maximal oxygen and carbon dioxide transport in anuran amphibians. J Appl Physiol 64:860–868PubMedGoogle Scholar
  58. Withers PC, Hillman SS (2001) Allometric and ecological relationships of ventricle and liver mass in anuran amphibians. Funct Ecol 15:60–69CrossRefGoogle Scholar
  59. Withers P, Hillman SS, Kimmel PB (1988) Effects of activity, hemorrhage, and dehydration on plasma catecholamine levels in the marine toad. Gen Comp Endocrinol 72:63–71PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of BiologyPortland State UniversityPortlandUSA

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