A meta-analysis of in vivo vertebrate cardiac performance: Implications for cardiovascular support in the evolution of endothermy

Journal of Experimental Biology

Volumn 218, Issue 8, 2015, Pages 1143-1150

  Hillman, Stanley S ^a   Hedrick, Michael S ^b  

^a PORTLAND STATE UNIVERSITY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Cardiac power; Exercise metabolism; Stroke work; Vascular conductance; Vertebrate exercise

Indexed keywords

ANIMAL; BASAL METABOLIC RATE; BLOOD PRESSURE; ENERGY METABOLISM; EVOLUTION; HEART; HEART OUTPUT; HEART STROKE VOLUME; META ANALYSIS; PHYSIOLOGY; THERMOGENESIS; VERTEBRATE;

ANIMALS; BASAL METABOLISM; BIOLOGICAL EVOLUTION; BLOOD PRESSURE; CARDIAC OUTPUT; ENERGY METABOLISM; HEART; STROKE VOLUME; THERMOGENESIS; VERTEBRATES;

EID: 84946013497     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.118372     Document Type: Article

References (55)

1. Andersen, P. and Saltin, B. (1985). Maximal perfusion of skeletal muscle in man. J. Physiol. 366, 233-249.
2. Axelsson, M. (1988). The importance of nervous and humoral mechanisms in the control of cardiac performance in the Atlantic cod Gadus morhua at rest and non-exhaustive exercise. J. Exp. Biol. 137, 287-303.
3. Axelsson, M. and Nilsson, S. (1986). Blood pressure regulation during exercise in the Atlantic cod Gadus morhua. J. Exp. Biol. 126, 225-236.
4. Axelsson, M., Driedzic, W. R., Farrell, A. P. and Nilsson, S. (1989). Regulation of cardiac output and gut blood flowinthe sea raven, Hemitripterus americanus. Fish Physiol. Biochem. 6, 315-326.
5. 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, 179-201.
6. Bennett, A. F. and Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science 206, 649-654.
7. Bishop, C. M. (1997). Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 447-456.
8. Bishop, C. M. (1999). The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc. R. Soc. Lond. B Biol. Sci. 266, 2275-2281.
9. Brooks, G. A., Fahey, T. D. and White, T. P. (1996). Exercise Physiology: Human Bioenergetics and Its Applications. Mt. View, USA: Mayfield Publishing.
10. Carey, C. (1979). Aerobic and anaerobic energy expenditure during rest and activity in montane Bufo b. boreas and Rana pipiens. Oecologia 39, 213-228.
11. Clarke, A. and Portner, H.-O. (2010). Temperature, metabolic power and the evolution of endothermy. Biol. Rev. 85, 703-727.
12. Conley, K. E., Christian, K. A., Hoppeler, H. and Weibel, E. R. (1995). Heart mitochondrial properties and aerobic capacity are similarly related in a mammal and a reptile. J. Exp. Biol. 198, 739-746.
13. Cowles, R. B. (1958). Possible origin of dermal temperature regulation. Evolution 12, 347-357.
14. Davie, P. S. and Forster, M. E. (1980). Cardiovascular responses to swimming in eels. Comp. Biochem. Physiol. A Physiol. 67, 367-373.
15. Dawson, T. J., Webster, K. N., Lee, E. and Buttemer, W. A. (2013). High muscle mitochondrial volume and aerobic capacity in a small marsupial (Sminthopsis crassicaudata) reveals flexible links between energy-use levels in mammals. J. Exp. Biol. 216, 1330-1337.
16. di Prampero, P. E. (2003). Factors limiting maximal performance in humans. Eur. J. Appl. Physiol. 90, 420-429.
17. Farrell, A. P. (1982). Cardiovascular changes in the unanaesthetized lingcod (Ophiodon elongatus) during short-term, progressive hypoxia and spontaneous activity. Can. J. Zool. 60, 933-941.
18. Frappell, P., Schultz, T. and Christian, K. (2002). Oxygen transfer during aerobic exercise in a varanid lizard Varanus mertensi is limited by the circulation. J. Exp. Biol. 205, 2725-2736.
19. Gallaugher, P. E. (1994). The role of hematocrit in oxygen transport in swimming salmonid fishes, pp. 279. PhD thesis, Department of Biological Sciences, Simon Fraser University, Burnaby.
20. Gallaugher, P. E., Thorarensen, H., Kiessling, A. and Farrell, A. P. (2001). Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming. J. Exp. Biol. 204, 2861-2872.
21. Grubb, B. A. (1982). Cardiac output and stroke volume in exercising ducks and pigeons. J. Appl. Physiol. 53, 207-211.
22. Grubb, B. A., Jorgensen, D. D. and Conner, M. (1983). Cardiovascular changes in the exercising emu. J. Exp. Biol. 104, 193-201.
23. Hedrick, M. S., Palioca, W. B. and Hillman, S. S. (1999). Effects of temperature and physical activityon blood flow shunts and intracardiac mixing in the toad Bufo marinus. Physiol. Biochem. Zool. 72, 509-519.
24. 2 uptake in rats selectively bred for endurance running capacity. J. Appl. Physiol. 93, 1265-1274.
25. Hillman, S. S., Hancock, T. V. and Hedrick, M. S. (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, 167-179.
26. Hillman, S. S., Hedrick, M. S. and Kohl, Z. F. (2014). Net cardiac shunts in anuran amphibians: physiology or physics? J. Exp. Biol. 217, 2844-2847.
27. Holroyd, S. M. and Gibbs, C. L. (1993). The energetics of shortening amphibian cardiac muscle. Pflugers Arch. 424, 84-90.
28. Johnston, I. A. and Moon, T. W. (1981). Fine structure and metabolism of multiply innervated fast muscle fibres in teleost fish. Cell Tissue Res. 219, 93-109.
29. Karas, R. H., Taylor, C. R., Rosler, K. and Hoppeler, H. (1987). Adaptive variation in the mammalian respiratory system in relation to energetic demand: V. Limits to oxygen transport by the circulation. Respir. Physiol. 69, 65-79.
30. 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.
31. Kohl, Z. F., Hedrick, M. S. and Hillman, S. S. (2013). Separating the contributions of vascular anatomy and blood viscosity to peripheral resistance and the physiological implications of interspecific resistance variation in amphibians. J. Comp. Physiol. B 183, 921-932.
32. Lai, N. C., Graham, J. B., Lowell, W. R. and Shebatai, R. (1989). Elevated pericardial pressure and cardiac output in the leopard shark, Triakis semifasciata, during exercise: the role of the percardioperitoneal canal. J. Exp. Biol. 147, 263-277.
33. Lai, N. C., Graham, J. B. and Burnett, L. (1990). Blood respiratory properties and the effect of swimming on blood gas transport in the leopard shark Triakis semifasciata. J. Exp. Biol. 151, 161-173.
34. Licht, P. (1965). Effects of temperature on heart rates of lizards during rest and activity. Physiol. Zool. 38, 129-137.
35. Lillywhite, H. B., Zippel, K. C. and Farrell, A. P. (1999). Resting and maximal heart rates in ectothermic vertebrates. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 124, 369-382.
36. Loiselle, D. S. and Gibbs, C. L. (1979). Species differences in cardiac energetics. Am. J. Physiol. 237, H90-H98.
37. Marsh, R. L. and Taigen, T. L. (1987). Properties enhancing aerobic capacity of calling muscles in gray tree frogs Hyla versicolor. Am. J. Physiol. 252, R786-R793.
38. McNab, B. K. (1978). The evolution of endothermy in the phylogeny of mammals. Am. Nat. 112, 1-21.
39. Overgaard, J., Andersen, J. L., Findsen, A., Pedersen, P. B. M., Hansen, K. Ozolina, K. and Wang, T. (2012). Aerobic scope and cardiovascular oxygen transport is not compromised at high temperatures in the toad Rhinella marina. J. Exp. Biol. 215, 3519-3526.
40. Peters, G. W., Steiner, D. A., Rigoni, J. A., Mascilli, A. D., Schnepp, R. W. and Thomas, S. P. (2005). Cardiorespiratory adjustments ofhoming pigeonstosteady wind tunnel flight. J. Exp. Biol. 208, 3109-3120.
41. Piiper, J., Meyer, M., Worth, H. and Willmer, H. (1977). Respiration and circulation during swimming activity in the dogfish Scyliorhinus stellaris. Respir. Physiol. 30, 221-239.
42. Pough, F. H. (1980). The advantages of ectothermy for tetrapods. Am. Nat. 115, 92-112.
43. 2max. J. Appl. Physiol. 66, 2491-2495.
44. Schaeffer, P. J., Conley, K. E. and Lindstedt, S. L. (1996). Structural correlates of speed and endurance in skeletal muscle: the rattlesnake shaker muscle. J. Exp. Biol. 199, 351-358.
45. Seymour, R. S. (1973). Physiological correlates of forced activity and burrowing in the spadefoot toad, Scaphiopus hammondii. Copeia 1973, 103-115.
46. Shiels, H. A. and Galli, G. L. J. (2014). The sarcoplasmic reticulum and the evolution of the vertebrate heart. Physiology 29, 456-469.
47. Stray-Gunderson, J., Musch, T. I., Haidet, G. C., Swain, D. P., Ordway, G. A. and Mitchell, J. H. (1986). The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circ. Res. 58, 523-530.
48. Tota, B., Acierno, R. and 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. R. Soc. Lond. B Biol. Sci. 332, 191-198.
49. Weibel, E. R. (2000). Symmorphosis: On Form and Function in Shaping Life. Cambridge, MA: Harvard University Press.
50. Weibel, E. R. and Hoppeler, H. (2005). Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J. Exp. Biol. 208, 1635-1644.
51. Weibel, E. R., Taylor, C. R. and Hoppeler, H. (1991). The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc. Natl. Acad. Sci. USA 88, 10357-10361.
52. Weibel, E. R., Baclgalupe, L. D., Schmitt, B. and Hoppeler, H. (2004). Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir. Physiol. Neurobiol. 140, 115-132.
53. West, N. H. and Smits, A. W. (1994). Cardiac output in conscious toads (Bufo marinus). J. Exp. Biol. 186, 315-323.
54. Withers, P. C. and Hillman, S. S. (1988). A steady-state model of maximal oxygen and carbon dioxide transport in anuran amphibians. J. Appl. Physiol. 64, 860-868.
55. Withers, P. C., Hillman, S. S., Simmons, L. A. and Zygmunt, A. C. (1988). Cardiovascular adjustments to enforced activity in the anuran amphibian, Bufo marinus. Comp. Biochem. Physiol. 89, 45-49.