A Perspective on the Evolution of the Coronary Circulation in Fishes and the Transition to Terrestrial Life

  • A. P. Farrell
  • N. D. Farrell
  • H. Jourdan
  • G. K. Cox


Coronary development in birds and mammals occurs in concert with myocardial compaction, likely in response to myocardial hypoxia. Furthermore, the degree of compaction of a cardiac chamber greatly reflects its work rate. These same driving forces likely featured prominently during the evolution of the coronary circulation among chordates. Yet, the means of supplying oxygen to fish hearts represent solutions that are far more diverse, possibly more complex and certainly more mysterious than those for the adult mammalian heart. To date, a coronary circulation has always been found associated with compact myocardium in fish; this is true for ventricle and the conus arteriosus. However, most fish species likely do not have a coronary circulation, nor do they have a thickened compact myocardium, and instead rely on the other oxygen supply route for the fish heart, the luminal oxygen supply to spongy myocardium. The archetype for the chambered vertebrate heart was likely avascular because no cyclostome has a coronary circulation. Nevertheless, the coronary circulation likely appeared when the first jawed vertebrates evolved because all extant elasmobranchs possess a coronary circulation that supplies the spongy and compact myocardial layers of the ventricle, as well as the compact myocardium of the conus. Extant species of basal teleosts provide evidence of a progressive evolutionary transition toward a loss of conal myocardium and the development of three forms of ventricular anatomy seen among modern day teleost species. The most prominent form is a reversion back to the archetypal spongy ventricle that lacks a coronary circulation. Most of the remaining teleosts have limited the coronary circulation to the outer compact myocardium and left the spongy myocardium avascular. A few species have a highly developed coronary system that serves both the spongy and compact myocardium, as in elasmobranchs. Thus, beyond the highly developed coronary circulations of endothermic sharks and tunas, cardiac evolution among fishes appears to have moved toward independence from a coronary circulation, beginning perhaps in the cyprinid lineage. Indeed, fish hearts comprise at least 30% and most often 100% spongy myocardium. Although air breathing in fishes increased the security of the luminal oxygen supply to the heart, it did not supplant the need for a coronary circulation. Many mysteries still remain regarding the coronary circulation in fishes including the extent to which the spongy myocardium is vascularized.


Coronary Blood Flow Coronary Vessel Coronary Circulation Myocardial Oxygen Demand Conal Myocardium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are deeply indebted to the courtesy shown to us by the staff of the Natural History Museum of London, UK, who provided open access to their fish collection and especially Oliver Crimmen, Patrick Campbell, James Maclain, and Ralf Britz. This work was by funded by the Natural Sciences and Engineering Council of Canada.


  1. Angelini A, Melancini P, Barbero F, Thiene G (1999) Evolutionary persistense of spongy myocardium in humans. Circulation 99:2475PubMedCrossRefGoogle Scholar
  2. Axelsson M (2005) The circulatory system and its control. In: Farrell AP, Steffensen JF (eds) Physiology of polar fishes. Fish physiology, vol 22. Elsevier, San DiegoGoogle Scholar
  3. Axelsson M, Farrell AP (1993) Coronary blood flow in vivo in the coho salmon (Oncorhynchus kisutch). Am J Physiol 264:R963–971PubMedGoogle Scholar
  4. Brill RW (1996) Selective advantages conferred by the high performance physiology of tunas, bilfishes, and dolphin fish. Comp Biochem Physiol 113A:3–15CrossRefGoogle Scholar
  5. Brill RW, Bushnell PG (2001) Tuna metabolism and energetics. In: Block BA, Stevens ED (eds) Tuna: physiology, ecology and evolution. Fish physiology, vol 19. Academic, San Diego, pp 79–120Google Scholar
  6. Budgett JS (1901) On some points in the anatomy of Polypterus. Trans Zool Soc Lond 15:323–341CrossRefGoogle Scholar
  7. Bushnell P, Jones DR, Farrell AP (1992) The arterial system. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol 12A. Academic, New York, pp 89–139Google Scholar
  8. Cox GK, Sandblom E, Farrell AP (2010a) Cardiac responses to anoxia in the Pacific hagfish, Eptatretus stoutii. J Exp Biol 213:3692–3698PubMedCrossRefGoogle Scholar
  9. Cox GK, Sandblom E, Richards JG, Farrell AP (2010b) Anoxic survival of the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 181:361–371PubMedCrossRefGoogle Scholar
  10. Davie PS (1990) Pacific Marlins. Anatomy and Physiology. Massey University Printery, Palmerston North, New ZealandGoogle Scholar
  11. Davie PS, Farrell AP (1991a) Cardiac performance of an isolated heart preparation from the dogfish (Squalus acanthias): the effects of hypoxia and coronary artery perfusion. Can J Zool 69:1822–1828CrossRefGoogle Scholar
  12. Davie PS, Farrell AP (1991b) The coronary and luminal circulations of the myocardium of fishes. Can J Zool 69:1993–2001CrossRefGoogle Scholar
  13. Davie PS, Franklin CE (1992) Myocardial oxygen consumption and mechanical efficiency of a perfused dogfish heart preparation. J Comp Physiol B 162:256–262PubMedCrossRefGoogle Scholar
  14. Daxboeck C (1982) Effect of coronary artery ablation on exercise performance in Salmo gairdneri. Can J Zool 60:375–381CrossRefGoogle Scholar
  15. De Andres AV, Muñoz-Chapuli R, Sans-Coma V, Garcia-Garrido L (1990) Anatomical studies of the coronary system in elasmobranchs: I. Coronary arteries in lamnoid sharks. Am J Anat 187:303–310PubMedCrossRefGoogle Scholar
  16. De Andres AV, Muñoz-Chapuli R, Sans-Coma V, Garcia-Garrido L (1992) Anatomical studies of the coronary system in elasmobranchs: II. Coronary arteries in hexanchoid, squaloid, and carcharhinoid sharks. Anat Rec 233:429–439PubMedCrossRefGoogle Scholar
  17. Duncker DJ, Bache RJ (2008) Regulation of coronary blood flow during exercise. Physiol Rev 88:1009–1086PubMedCrossRefGoogle Scholar
  18. Emery SH, Mangano C, Randazzo V (1985) Ventricle morphology in pelagic elasmobranch fishes. Comp Biochem Physiol A 82:635–643PubMedCrossRefGoogle Scholar
  19. Fänge R (1986) Lymphoid organs in sturgeons (Acipenseridae). Vet Immunol Immunop 12:153–161CrossRefGoogle Scholar
  20. Farmer C (1997) Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates? Paleobiology 23:358–372Google Scholar
  21. Farmer CG (1999) Evolution of the vertebrate cardio-pulmonary system. Annu Rev Physiol 61:573–592PubMedCrossRefGoogle Scholar
  22. Farrell AP (1987) Coronary flow in a perfused rainbow trout heart. J Exp Biol 129:107–123PubMedGoogle Scholar
  23. Farrell AP (1991) From hagfish to tuna: a perspective on cardiac function in fish. Physiol Zool 64:1137–1164Google Scholar
  24. Farrell AP (1996) Features heightening cardiovascular performance in fishes, with special reference to tunas. Comp Biochem Physiol A 113:61–67CrossRefGoogle Scholar
  25. Farrell AP (1997) Evolution of cardiovascular systems: insights into ontogeny. In: Burggren WW, Keller B (eds) Development of the cardiovascular system: molecules to organisms. Cambridge University Press, Cambridge, pp 101–113Google Scholar
  26. Farrell AP (2007) Cardiovascular systems in primitive fishes. In: McKenzie DJ, Farrell AP, Brauner CJ (eds) Primitive fishes. Fish physiology, vol 26. Academic, San Diego, pp 53–120Google Scholar
  27. Farrell AP, Clutterham SM (2003) On-line venous oxygen tensions in rainbow trout during graded exercise at two acclimation temperatures. J Exp Biol 206:487–496PubMedCrossRefGoogle Scholar
  28. Farrell AP, Jones DR (1992) The heart. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol 12A. Academic, San Diego, pp 1–88Google Scholar
  29. 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
  30. Farrell AP, Steffensen JF (1987) Coronary ligation reduces maximum sustained swimming speed in Chinook salmon, Oncorhynchus tshawytscha. Comp Biochem Physiol A 87(1):35–37PubMedCrossRefGoogle Scholar
  31. Farrell AP, Hammons AM, Graham MS, Tibbits GF (1988) Cardiac growth in rainbow trout, Salmo gairdneri. Can J Zool 66:2368–2373CrossRefGoogle Scholar
  32. Farrell AP, Davie PS, Franklin CE, Johansen JA, Brill RW (1992) Cardiac physiology in tunas I: in vitro perfused heart preparations from yellowfin and skipjack tunas. Can J Zool 70:1200–1210CrossRefGoogle Scholar
  33. Farrell AP, Gamperl AK, Francis ETB (1998) Comparative aspects of heart morphology. In: Gans C, Gaunt AS (eds) Biology of the Reptilia, vol 19. Society for the Study of Amphibians and Reptiles, Ithaca, pp 375–424Google Scholar
  34. Farrell AP, Simonot DL, Seymour RS, Clark TD (2007) 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 71:389–398CrossRefGoogle Scholar
  35. Farrell AP, Eliason EJ, Sandblom E, Clark TD (2009) Fish cardiorespiratory physiology in an era of climate change. Can J Zool 87:835–851CrossRefGoogle Scholar
  36. Forster ME (1989) Performance of the heart of the hagfish, Eptatretus cirrhatus. Fish Physiol Biochem 6:327–331CrossRefGoogle Scholar
  37. Forster ME (1991) Myocardial oxygen consumption and lactate release by the hypoxic hagfish heart. J Exp Biol 156:583–590Google Scholar
  38. Forster ME, Davison W, Axelsson M, Farrell AP (1992) Cardiovascular responses to hypoxia in the hagfish, Eptatretus cirrhatus. Respir Physiol 88:373–386PubMedCrossRefGoogle Scholar
  39. Foxon GE (1950) A description of the coronary arteries in dipnoan fishes and some remarks on their importance from the evolutionary standpoint. J Anat 84:121–131PubMedGoogle Scholar
  40. Franklin CE, Davie PS (1992) Dimensional analysis of the ventricle of an in situ perfused trout heart using echocardiography. J Exp Biol 166:47–60PubMedGoogle Scholar
  41. Gamperl AK, Farrell AP (2004) Cardiac plasticity in fishes: environmental influences and intraspecific differences. J Exp Biol 207:2539–2550PubMedCrossRefGoogle Scholar
  42. Gamperl A, Pinder A, Grant R, Boutilier R (1994) Influence of hypoxia and adrenaline administration on coronary blood flow and cardiac performance in seawater rainbow trout (Oncorhynchus mykiss). J Exp Biol 193:209–232PubMedGoogle Scholar
  43. Gamperl AK, Axelsson M, Farrell AP (1995) Effects of swimming and environmental hypoxia on coronary blood flow in rainbow trout. Am J Physiol 269:R1258–1266PubMedGoogle Scholar
  44. Goo S, Joshi P, Sands G, Gerneke D, Taberner A, Dollie Q, LeGrice I, Loiselle D (2009) Trabeculae carneae as models of the ventricular walls: implications for the delivery of oxygen. J Gen Physiol 134:339–350PubMedCrossRefGoogle Scholar
  45. Graham JB (1997) Air-breathing fishes. Evolution, diversity and adaptation. Academic, San DiegoGoogle Scholar
  46. Grant RT, Regnier M (1926) The comparative anatomy of the cardiac coronary vessels. Heart J Stud Circ 8:285–317Google Scholar
  47. Greer Walker M, Santer RM, Benjamin M, Norman D (1985) Heart structure of some deep-sea fish (Teleostei: Macrouridae). J Zool Lond A 205:75–89CrossRefGoogle Scholar
  48. Grimes AC, Kirby ML (2009) The outflow tract of the heart in fishes: anatomy, genes and evolution. J Fish Biol 74:983–1036PubMedCrossRefGoogle Scholar
  49. Guerrero A, Icardo JM, Duran AC, Gallego A, Domezain A, Colvee E, Sans-Coma V (2004) Differentiation of the cardiac outflow tract components in alevins of the sturgeon Acipenser naccarii (Osteichthyes, Acipenseriformes): implications for heart evolution. J Morphol 260:172–183PubMedCrossRefGoogle Scholar
  50. Hagensen MK, Abe AS, Falk E, Wang T (2008) Physiological importance of the coronary arterial blood supply to the rattlesnake heart. J Exp Biol 211:3588–93PubMedCrossRefGoogle Scholar
  51. Halpern MH, May MM (1958) Phylogenetic study of the extracardiac arteries to the heart. Am J Anat 102:469–481PubMedCrossRefGoogle Scholar
  52. Hansen CA, Sidell BD (1983) Atlantic hagfish cardiac muscle: metabolic basis of tolerance to anoxia. Am J Physiol 244:R356–R362PubMedGoogle Scholar
  53. Holeton GF, Randall DJ (1967) The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout. J Exp Biol 46:317–327PubMedGoogle Scholar
  54. Hu N, Sedmera D, Yost HJ, Clark EB (2000) Structure and function of the developing zebrafish heart. Anat Rec 260:148–157PubMedCrossRefGoogle Scholar
  55. Icardo JM (1990) Development of the outflow tract. A study in hearts with situs solitus and situs inversus. Ann NY Acad Sci 588:26–40PubMedCrossRefGoogle Scholar
  56. Icardo JM (1996) Developmental biology of the vertebrate heart. J Exp Zool 275:144–161PubMedCrossRefGoogle Scholar
  57. Icardo JM, Colvee E, Cerra MC, Tota B (1999) Bulbus arteriosus of the Antarctic teleosts. I. The white-blooded Chionodraco hamatus. Anat Rec 254:396–407PubMedCrossRefGoogle Scholar
  58. Icardo JM, Colvee E, Cerra MC, Tota B (1999) Bulbus arteriosus of the Antarctic teleosts. II. The red-blooded Trematomus bernacchii. Anat Rec 256:116–126PubMedCrossRefGoogle Scholar
  59. Icardo JM, Guerrero A, Duran AC, Domezain A, Colvee E, Sans-Coma V (2004) The development of the sturgeon heart. Anat Embryol 208:439–449PubMedCrossRefGoogle Scholar
  60. Icardo JM, Amelio D, Garofalo F, Colvee E, Cerra MC, Wong WP, Tota B, Ip YK (2008) The structural characteristics of the heart ventricle of the African lungfish Protopterus dolloi: freshwater and aestivation. J Anat 213:106–119PubMedCrossRefGoogle Scholar
  61. Icardo JM, Guerrero A, Duran AC, Colvee E, Domezain A, Sans-Coma V (2009) The development of the epicardium in the sturgeon Acipenser naccarii. Anat Rec 292:1593–1601CrossRefGoogle Scholar
  62. Ilves KL, Randall DJ (2007) Why have primitive fishes survived? In: McKenzie DJ, Farrell AP, Brauner C (eds) Primitive fishes. Fish physiology, vol 26. Academic, San Diego, pp 515–536Google Scholar
  63. Jensen B, Nielsen JM, Axelsson M, Pedersen M, Lofman C, Wang T (2010) How the python heart separates pulmonary and systemic blood pressures and blood flows. J Exp Biol 213:1611–1617PubMedCrossRefGoogle Scholar
  64. Johansen K (1965) Cardiovascular dynamics in fishes, amphibians, and reptiles. Ann NY Acad Sci 127:414–442PubMedCrossRefGoogle Scholar
  65. Korsmeyer KE, Dewar H, Lai NC, Graham JB (1996) The aerobic capacity of tunas: adaptation for multiple metabolic demands. Comp Biochem Physiol A 113:17–24CrossRefGoogle Scholar
  66. McKenzie DJ, Farrell AP, Brauner CJ (eds) (2007) Primitive fishes. Fish physiology, vol 26. Academic, San DiegoGoogle Scholar
  67. Millot J, Anthony J, Robineau D (1978) Anatomie de Latimeria chalumnae. Tome 3, Appareils digestifs, respiratoire, urogenetal, circulatoire, glandes endocrine, teguments, ecailles, conclusions generales. Paris, Editions de Centre National de Rech. Scient., 198 ppGoogle Scholar
  68. Muñoz-Chapuli R, De Andres AV, Dingerkus G (1994) Coronary artery anatomy and elasmobranch phylogeny. Acta Zool Stockholm 75:249–254CrossRefGoogle Scholar
  69. O’Donogue CH, Abbot E (1928) The blood vascular sustem of the spiny dogfish Squlaus acanthias and Squalus sucklii. Trans R Soc Edinb 55:823–890Google Scholar
  70. Ostadal B, Schieble Th (1971) Terminal blood bed in heart of fish. Z Anat Entwicklungs 134:101–110CrossRefGoogle Scholar
  71. Parker TJ (1886) On the blood vessels of Mustelus anataricus. Phil Trans R Soc Lond Biol 177:685–732CrossRefGoogle Scholar
  72. Parker GH, Davis FK (1899) The blood vessels of the heart of Carachias, Raja and Amia. Proc Boston Soc Nat Hist 29:163–178Google Scholar
  73. Pieperhoff S, Bennett W, Farrell AP (2009) The intercellular organization of the two muscular systems in the adult salmonid heart, the compact and the spongy myocardium. J Anat 215:536–547PubMedCrossRefGoogle Scholar
  74. Poupa O, Gesser H, Jonsson S, Sullivan L (1974) Coronary supplied compact shell of ventricular myocardium in salmonids: growth and enzyme pattern. Comp Biochem Physiol A 48:85–95PubMedCrossRefGoogle Scholar
  75. Pratt FH (1898) The nutrition of the heart through the vessels of Thebesius and coronary veins. Am J Physiol 1:86–103Google Scholar
  76. Romenskii O (1978) Blood supply of the compact and spongy myocardium of fish, amphibia and reptiles. Arkh Anat Gistol Embriol 75:91–95PubMedGoogle Scholar
  77. Sanchez-Quintana D, Hurle JM (1987) Ventricular myocardial architecture in marine fishes. Anat Rec 217:263–273PubMedCrossRefGoogle Scholar
  78. Santer RM (1985) Morphology and innervation of the fish heart. Adv Anat Embryol Cell Biol 89:1–99PubMedCrossRefGoogle Scholar
  79. Santer RM, Greer Walker M (1980) Morphological studies on the ventricle of teleost and elasmobranch hearts. J Zool 190:259–272CrossRefGoogle Scholar
  80. Satchell GH (1991) Physiology and form of fish circulation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  81. Saunders RL, Farrell AP, Knox DE (1992) Progression of coronary arterial lesions in Atlantic salmon (Salmo salar) as a function of growth rate. Can J Fish Aquatic Sci 49:878–884CrossRefGoogle Scholar
  82. Sedmera D, Watanabe M (2006) Growing the coronary tree: the quail saga. Anat Rec A 288:933–935Google Scholar
  83. Sedmera D, Pexieder T, Vuillemin M, Thompson RP, Anderson RH (2000) Developmental patterning of the myocardium. Anat Rec 258:319–337PubMedCrossRefGoogle Scholar
  84. Seymour RS, Farrell AP, Christian K, Clark TD, Bennett MB, Wells RM, Baldwin J (2007) Continuous measurement of oxygen tensions in the air-breathing organ of Pacific tarpon (Megalops cyprinoides) in relation to aquatic hypoxia and exercise. J Comp Physiol B 177:579–587PubMedCrossRefGoogle Scholar
  85. Shipman B (1989) Patterns of ventilation and acid-base recovery following exhausting activity in the air-breathing fish Lepisosteus oculatus. M.Sc. Thesis. University of Texas, ArlingtonGoogle Scholar
  86. Stainier DY, Lee RK, Fishman MC (1993) Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. Development 119:31–40PubMedGoogle Scholar
  87. Sugishita Y, Watanabe M, Fisher SA (2004) Role of myocardial hypoxia in remodeling of the embryonic avian cardiac outflow tract. Dev Biol 267:294–308PubMedCrossRefGoogle Scholar
  88. Thebesius AC (1708) Dissertatio Medica de Cirulo Sanguinis in Corde. Elsevier, Lugduni BatacorumGoogle Scholar
  89. Tomanek RJ (1996) Formation of the coronary vasculature: a brief review. Cardiovasc Res 31:E46–E51PubMedGoogle Scholar
  90. Tota B (1978) Functional cardiac morphology and biochemistry in Atlantic bluefin tuna. In: Sharp GD, Dizon AE (eds) The physiological ecology of tunas. Academic, New York, pp 89–112Google Scholar
  91. Tota B (1983) Vascular and metabolic zonation in the ventricular myocardium of mammals and fishes. Comp Biochem Physiol A 76:423–437PubMedCrossRefGoogle Scholar
  92. Tota B (1989) Myoarchitecture and vascularization of the elasmobranch heart ventricle. J Exp Zool:122–135Google Scholar
  93. Tota B, Cimini V, Salvatore G, Zummo G (1983) Comparative study of the arterial and lacunary systems of the ventricular myocardium of elasmobranch and teleost fishes. Am J Anat 167:15–32PubMedCrossRefGoogle Scholar
  94. Tota B, Acierno R, Agnisola C (1991) Mechanical Performance of the isolated and perfused heart of the haemoglobinless Antarctic icefish Chionodraco hamatus (Lonnberg): effects of loading conditions and temperature. Philos Trans Roy Soc B 332:191–198CrossRefGoogle Scholar
  95. Van Citters RL, Watson NW (1967) Coronary disease in spawning steelhead trout, Salmo gairdneri. Science 159:105–107CrossRefGoogle Scholar
  96. Voboril Z, Schieble T (1970) Blood supply of turtle heart. Z Anat Entwicklungs 130:95–98CrossRefGoogle Scholar
  97. Wanga J, Eckberg WR, Anderson WA (2001) Ultrastructural differentiation of cardiomyocytes of the zebrafish during the 8-26-somite stages. J Submicrosc Cytol Pathol 33:275–287PubMedGoogle Scholar
  98. Wells RMG, Forster ME, Davison W, Taylor HH, Davie PS, Satchell GH (1986) Blood oxygen transport in the free swimming hagfish, Eptatretus cirrhatus. J Exp Biol 123:43–53PubMedGoogle Scholar
  99. Zaccone D, Grimes AC, Sfacteria A, Jaroszewska M, Caristina G, Manganaro M, Farrell AP, Zaccone G, Dabrowski K, Marino F (2011) Complex innervation patterns of the conus arteriosus in the heart of the longnose gar, Lepisosteus osseus. Acta Histochem 113:578–584PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • A. P. Farrell
    • 1
  • N. D. Farrell
    • 1
  • H. Jourdan
    • 1
  • G. K. Cox
    • 1
  1. 1.Department of ZoologyUniversity of British ColumbiaVancouverCanada

Personalised recommendations