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Physiological states and intracardiac shunting in non-crocodilian reptiles

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EBO — Experimental Biology Online Annual 1996/97

Part of the book series: EBO — Experimental Biology Online Annual ((EBOEXP,volume 1996/1997))

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Abstract

Historically, the evolution of the vertebrate heart was portrayed as a continuous progression from the two-chambered heart of fish to the completely divided, four-chambered heart of birds and mammals. The incompletely divided ventricle of non-crocodilian reptiles and the resulting central mixing of oxygen-rich and oxygen-poor blood (cardiac shunting) was viewed as an intermediate phylogenetic step that was functionally inefficient compared to the circulation of “higher” vertebrates. This perception changed when studies showed that the degree of mixing within the reptilian heart is influenced by the ventilatory state of the animal and is regulated by the autonomic nervous system. The ability to control cardiac shunts is hypothesized to provide several unique physiological advantages to reptiles and has given rise to the notion that cardiac shunting is a highly derived condition, representing a successful adaptation for animals with low metabolic rates and intermittent breathing patterns. The modern view of the reptilian circulation is based, to a large measure, on a relatively small number of observations during very specific types of behaviors or physiological states, being primarily restricted to the description of cardiovascular changes associated with intermittent lung ventilation. The goals of this review are to summarize the studies that have described cardiac shunting patterns in non-crocodilian reptiles during a variety of physiological states and to emphasize the need for additional research on this important group of vertebrates.

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References

  • Ackerman, R., White, F.N.(1979) Cyclic carbon dioxide exchange in the turtle, Pseudemys scripta. Physiol. Zool. 52: 378-389

    Google Scholar 

  • Axelsson, M., Fritsche, R., Holmgren, S., Grove, D.J., Nilsson, S. (1991) Gut blood flow in the esturine crocodile,Crocodylus porosus. Acta Physiol. Scand. 142:(2) 509-516

    Article  PubMed  CAS  Google Scholar 

  • Baker, L.A., White, F.N. (1970) Redistribution of cardiac output in response to heating in Iguana iguana. 35: 253-262

    Google Scholar 

  • Benedict, F. G. (1932) The physiology of large reptiles. Carnegie Institute Washington Publ. 425

    Google Scholar 

  • Berger, P.J., Burnstock, G. (1979) Autonomic nervous system. In: Gans, C., Northcutt, G., Ulinksi, P. (eds.) Biology of the reptilia., Vol.10. Neurology. Academic Press, New York, pp.1-47

    Google Scholar 

  • Brücke, E. (1852) Beiträge zur vergleichenden Anatomie und Physiologie des Gefäßsystems. Denkschr Akad Wien 3: 335–367

    Google Scholar 

  • Burggren, W. (1975) A quantitative analysis of ventilation tachycardia and its control in two chelonians, Pseudemys scripta and Testudo graeca. J. Exp. Biol. 63: 367–380

    CAS  Google Scholar 

  • Burggren, W. (1977) The pulmonary circulation of the chelonian reptile: morphology, pharmacology and hemodynamics. J. Comp. Physiol. B. 116: 303–324

    Article  CAS  Google Scholar 

  • Burggren, W. (1985) Hemodynamics and regulation of central cardiovascular shunts in reptiles. In: Johansen, K., Burggren, W. (eds.) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp. 121–142

    Google Scholar 

  • Burggren, W., Johansen, K. (1982) Ventricular hemodynamics in the monitor lizard, Varanus exanthematicus, pulmonary and systemic pressure separation. J. Exp. Biol. 96: 343–354

    Google Scholar 

  • Burggren, W.W., Warburton, S.J. (1994) Patterns of form and function in developing hearts: contributions from non-mammalian vertebrates. Cardioscience 5: 183–191

    PubMed  CAS  Google Scholar 

  • Burrgen, W., Smits, A., Evans, B. (1989) Arterial 02 homeostasis during diving in the turtle Chelodina longicollis. Physiol. Zool. 62: 668–686

    Google Scholar 

  • Butler, P., Milsom, W.K, Woakes, A.J. (1984) Respiratory, cardiovascular and metabolic adjustments during steady state swimming in the green turtle, Chelonia mydas. J. Comp. Physiol. B 154: 167–74

    Article  Google Scholar 

  • Comeau, S.G., Hicks, J.W. (1994) Regulation of central vascular blood flow in the turtle. Am. J. Physiol 36: R569–R578

    Google Scholar 

  • Comeau, S., Lance, V.A., Hicks, J.W., Conlon, J.M. (1992) Purification and biological activity of alligator bradykinin. Am. J. Physiol. 263: R400-R404

    PubMed  CAS  Google Scholar 

  • Conlon, J.M., Hicks, J.W., Smith, D.D. (1990) Isolation and biological acitivty of a novel kinin ([Thr6]) bradykinin from the turtle, Pseudemys scripta. Endocrinology 126: 985-991

    Article  CAS  Google Scholar 

  • Douglas, C.G., Haldane, J.S. (1922) The regulation of the general circulation rate in man. J. Physiol. (Lond) 56:69-l00

    CAS  Google Scholar 

  • Foxon, G.E.H.(1955) Problems of the double circulation in vertebrates. Biol. Rev. 30:196-228

    Article  Google Scholar 

  • Gatten, R.E. (1975) Effects of activity on blood oxygen saturation, lactate and pH in the turtles Pseudemys scripta and Terrapene ornata. Physiol. Zool. 48: 24–35.

    CAS  Google Scholar 

  • Gleeson, T.T., Mitchell, G.S., Bennett, A.F. (1980) Cardiovascular responses to graded activity in the lizards Varanus andlguana. Am. J. Physiol. 239: R174–R179

    PubMed  CAS  Google Scholar 

  • Griel, A. (1903) Beiträge zur vergleichenden Anatomie und Entwicklungsgeschicte des Herzens und des Truncus arteriosis der Wirbelthiere. Morphol. Jahrb. 31: 123-310

    Google Scholar 

  • Grigg, G.C., Johansen, K. (1987) Cardiovascular dynamics in Crododylus porosus breathing air and during voluntary aerobic dives. J. Comp. Physiol. B 157: 381–392

    Article  Google Scholar 

  • Heisler, N., Glass, M.L (1985) Mechanisms and regulation of central vascular shunts in reptiles. In: Johansen, K., Burggren, W. (eds.) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp. 334-353

    Google Scholar 

  • Hicks, J.W. (1993) Regulation of intracardiac shunting in reptiles: anatomic vs effective shunting. In: Bicudo, J.E., Glass, M.L. (eds.) The vertebrate gas transport cascade: adaptations to environment and mode of life. CRC Press, Boca Raton, pp. 252–265

    Google Scholar 

  • Hicks, J.W. (1994) Adrenergic and cholinergic regulation of intracardiac shunting in chelonias. Physiol. Zool. 67: 1325–1346

    Google Scholar 

  • Hicks, J.W., Comeau, S.G. (1994) Vagal regulation of intracardiac shunting in the turtle Pseudemys scrip ta. J. Exp. Biol. 186: 109-126

    PubMed  Google Scholar 

  • Hicks, J.W., Malvin, G.M. (1992) Mechanism of intracardiac shunting in the turtle Pseudemys scripta. Am. J. Physiol. 262: R986–R992

    PubMed  CAS  Google Scholar 

  • Hicks, J.W., Malvin, G.M. (1996) Mechanism of intracardiac shunting in reptiles: pressure vs washout shunting. In: Heisler, N. (ed.) Advances in comparative and environmental physiology, mechanisms of systemic regulation. Vol I. Respiration and circulation. Springer, Berlin Heidelberg New York, pp. 137-155

    Google Scholar 

  • Hicks, J.W., White, F.N. (1992) Ventilation and gas exchange during intermittent ventilation in the American alligator, Alligator mississipiensis. Respir. Physiol. 88: 23-36

    Article  PubMed  CAS  Google Scholar 

  • Hicks, J.W., Wang, T. (1996) The functional role of cardiac shunts in reptiles. J. Exp. Zool. (in press)

    Google Scholar 

  • Hicks, J.W., Wood S.C. (1989) Oxygen homeostasis in lower vertebrates: the impact of external and internal hypoxia. In: Wood, S.C. (ed.) Lung biology in health and disease-comparative pulmonary physiology: current concepts. Marcel Dekker, New York, pp. 311–341

    Google Scholar 

  • Hicks, J.W., Ishimatsu, A., Molloi, S., Erashin, A., Heisler, N. (1996) The mechanism of cardiac shunting in reptiles: a new synthesis. J. Exp. Biol. (in press)

    Google Scholar 

  • Hopkins, S., Hicks, J.W., Cooper, T., Powell, F. (1995) Ventilation-perfusion relations in the savannah monitor during treadmill exercise. J. Exp. Biol. 198: 1783–1789

    Google Scholar 

  • Hopkins, S.R., Wang, T., Hicks., J.W. (1995) Ventilation-perfusion heterogeneity improves with increased pulmonary blood flow in anaesthetized turtles. FASEB J 9: (4) A641, abstr. no. 3716

    Google Scholar 

  • Hopkins, S.R., Wang, T., Hicks, J.W. (1996) The effects of altering pulmonary blood flow on pulmonary gas exchange in the turtle Trachemys (Pseudemys) scripta. J. Exp. Biol. (in press)

    Google Scholar 

  • Houlihan, D. F. (1991) Protein turnover in ectotherms and its relationships to energetics. Adv. Comp. Environ. Physiol. 7: 1–43

    Article  CAS  Google Scholar 

  • Ishimatsu, A., Hicks, J.W., Heisler, N. (1988) Analysis of intracardiac shunting in the lizard, Varanus niloticus: a new model based on blood oxygen levels and microsphere distribution. Respir. Physiol. 71: 83–100

    Article  PubMed  CAS  Google Scholar 

  • Ishimatsu, A., Hicks, J.W., Heilser, N. (1996) Analysis of intracardiac shunting in the turtle, Trachemys (Pseudemys) scripta: application of the three outflow vessel model. J. Exp. Biol. (in press)

    Google Scholar 

  • Johansen, K., Burggren, W.W. (1980) Cardiovascular function in lower vertebrates. In: Hearts and hart like organs. Academic Press, New York, pp. 61–117

    Google Scholar 

  • Jones, D.R., Shelton, G. (1993) The physiology of the alligator heart: left aortic flow patterns and right-to-left shunts. J. Exp. Biol. 176: 247–269

    Google Scholar 

  • Kooyman, G.L. (1989) Diverse divers, physiology and behavior. Springer, Berlin Heidelberg New York

    Book  Google Scholar 

  • Krosniunas, E., Hicks, J.W. (1994) Cardiovascular correlates of behavior in the turtle (abstract). The Physiologist A-95, abstr. no. 58. 24

    Google Scholar 

  • Krosniunas, E., Hicks, J.W. (1995) Intracardiac shunts during voluntary activity and rest in the turtle (abstract). Am. Zool. 35: A63, abstr. no. 253

    Google Scholar 

  • Lillywhite, H.B., Donald, J.A. (1989) Pulmonary blood flow regulation in an aquatic snake. Science 245: 293-295

    Google Scholar 

  • Lister, G., Pitt, B.R. (1983) Cardiopulmonary interactions in the infant with congenital cardiac disease. Clin. Chest Med. 4: 219–232

    PubMed  CAS  Google Scholar 

  • Luckhardt, A.B., Carlson, A.J. (1921) Studies on the visceral sensory nervous system. VIII. On the presence of vasomotor fibres in the vagus nerve to the pulmonary vessels of the amphibian and reptilian lung. Am. J. Physiol. 56: 72–112

    Google Scholar 

  • Mathur, P.N. (1946) The anatomy of the reptilian heart. II. Serpentes, Testudinata and Loricata. Proc. Indian Acad. Sci. 20: 1–29

    Google Scholar 

  • Millard, R.W., Johansen, K. (1973) Ventricular outflow dynamics in the lizard, Varanus niloticus: responses to hypoxia, hypercarbia and diving. J. Exp. Biol. 60: 871–880

    Google Scholar 

  • Millen, J.E., Murdaugh, H.V., Bauer, C.B., Robin, D. (1964) Circulatory adaptation to diving in the freshwater turtle. Science 145: 591-593

    Google Scholar 

  • Milsom, W.K., Langille, B.L., Jones, D.R. (1977) Vagal control of pulmonary

    Google Scholar 

  • vascular resistance in the turtle Chrysemys scripta. Can. J. Zool. 55: 359-367

    Google Scholar 

  • Mitchell, G. S., Gleeson, T. T., Bennett, A. F. (1981a) Ventilation and acid-base balance during graded activity in lizards. Am. J. Physiol. 240: R29–R37

    PubMed  CAS  Google Scholar 

  • Mitchell, G. S., Gleeson, T. T., Bennett, A. F. (1981b) Pulmonary 02 transport during activity in lizards. Respir. Physiol. 43: 365-375

    Google Scholar 

  • Mithoefer, J.C.(1959) Mechanism of pulmonary gas exchange and CO2 transport during breath holding. J. Appl. Physiol. 14:706-710

    Google Scholar 

  • Nilsson, S. (1983) Autonomic nerve function in the vertebrates. Springer, New York Berl in Heidelberg

    Book  Google Scholar 

  • Donoghue, C.H. (1918) The heart of the leathery turtle, Dermochelys (Sphargis) coriacea. With a note on the septum ventriculorum in the Reptilia. J. Anat. Lond. 52: 823–890

    Google Scholar 

  • Otis, A.B., Rahn, H., Fenn, W.O. (1948) Alveolar gas exchange during breath holding. Am. J. Physiol. 152: 674–686

    PubMed  CAS  Google Scholar 

  • Rau, A.S. (1924) Observations of the anatomy of the heart of Tiliqua scincoides and Eunectes murinus. J. Anat. Lond. 59: 60–71

    CAS  Google Scholar 

  • Secor, S. M., Diamond, J. (1995) Adaptive responses to feeding in Burmese pythons: pay before pumping J. Exp. Biol. 198: 1313-1325

    Google Scholar 

  • Secor, S.M., Stein, E.D., Diamond, J. (1994) Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation. Am. J. Physiol. 266: G695-G705

    Google Scholar 

  • Shelton, G., Burggren, W.W. (1976) Cardiovascular dynamics of the Chelonia during apnea and lung ventilation. J. Exp. Biol. 64: 323-343

    Google Scholar 

  • Shelton, G., Jones, D.R., Milsom, W.K. (1986) Control of breathing in ectothermic vertebrates. In: Handbook of physiology. Section 3: The respiratory system. Vol. H. American Physiological Society, Bethesda, pp. 857-909

    Google Scholar 

  • Sievert, L.M., Sievert, G.A., Cupp, P.V. (1988) Metabolic rate of feeding and fasting juvinile midland painted turtles, Chrysemys picta marginata. Comp. Biochem. Physiol. 90A: 157–161

    Google Scholar 

  • Steggerda F.R., Essex, H.E. (1957) Circulation and blood pressure in the great vessels and heart of the turtle Chelydra serpentina. Am. J. Physiol. 190: 320–326.

    CAS  Google Scholar 

  • Templeton, R. (1970) Comparative physiology of thermoregulation. Whittow, G.C. (ed.). Academic Press, New York, Chapter 5, pp. 167–221

    Google Scholar 

  • Van Mierop, L.H.S., Kutsche L.M. (1981) Comparative anatomy of the ventricular septum. In: Wenink, A.C.G. (ed.) The ventricular septum of the heart. Martinus Nijhoff, The Hague, pp. 35-46

    Google Scholar 

  • Van Mierop, L.H.S., Kutsche, L.M. (1985) Some aspects of comparative anatomy of the heart. In: Johansen, K., Burggren, W. (eds.) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp. 38–56

    Google Scholar 

  • Wang, T., Hicks, J.W. (1994) Hypoxia and reduced blood hemoglobin concentration elicits left-to-right cardiac shunting in the turtle (abstract). The Physiologist A-95, abstr. no. 58. 21

    Google Scholar 

  • Wang, T., Hicks, J.W. (1996a) The interaction of pulmonary ventilation and cardiac shunts on arterial oxygen levels. J. Exp. Biol. (in press)

    Google Scholar 

  • Wang, T., Hicks, J.W. (1996b) Cardiorespiratory synchrony in the turtle. J. Exp. Biol. (in press)

    Google Scholar 

  • Webb, G., Heatwole, H., Bavay, J. de (1971) Comparative cardiac anatomy of the Reptilia. I. The chambers and septa of the varanid ventricle. J. Morphol. 134: 335-350

    Article  PubMed  CAS  Google Scholar 

  • Webb, G., Heatwole, H., Bavay, J. de (1974) Comparative cardiac anatomy of the Reptilia. II. A critique of the literature on the Squamata and Rhynchocephalia. J. Morphol. 142: 1–20

    Article  PubMed  CAS  Google Scholar 

  • West, N., Butler, P.J., Bevan, R.M. (1992) Pulmonary blood flow at rest and during swimming in the green turtle, Chelonia mydas. Physiol. Zool. 65: 287–310

    Google Scholar 

  • White, F.N.(1959) Circulation in the reptilian heart (Squamata). Anat. Rec. 1 35: 129-134

    Google Scholar 

  • White, F.N. (1968) Functional anatomy of the heart of reptiles. Am. Zool. 8: 211–219

    PubMed  CAS  Google Scholar 

  • White, F.N. (1970) Central vascular shunts and their control in reptiles. Fed. Proc. Fed. Soc. Exp. Biol. 29: 1149–1153

    Google Scholar 

  • White, F.N. (1976) Circulation. In: Gans, C., Dawson, W.R. (eds.) Biology of the reptilia. Academic Press, New York, pp. 275–334

    Google Scholar 

  • White, F.N. (1985) Role of intracardiac shunts in pulmonary gas exchange in chelonian reptiles. In: Johansen, K., Burggren, W. (eds.) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp. 296–309

    Google Scholar 

  • White, F.N., Ross, G. (1966) Circulatory changes during experimental diving in the turtle. Am. J. Physiol. 211: 15–18

    PubMed  CAS  Google Scholar 

  • White, F.N., Hicks, J.W., Ishimatsu, A. (1989) Respiratory states and intracardiac shunts in turtles. Am. J. Physiol. 256: R240–R247

    PubMed  CAS  Google Scholar 

  • Withers, P.C. (1992) Comparative animal physiology. Saunders, Philadelphia

    Google Scholar 

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA, 92717, USA

    James W. Hicks

  2. Department of Biologic and Materials Science, School of Dentistry, University of Michigan, Ann Arbor, MI, 48109-1078, USA

    Egle Krosniunas

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  1. James W. Hicks
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  2. Egle Krosniunas
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Hicks, J.W., Krosniunas, E. (1998). Physiological states and intracardiac shunting in non-crocodilian reptiles. In: EBO — Experimental Biology Online Annual 1996/97. EBO — Experimental Biology Online Annual, vol 1996/1997. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-00932-1_3

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  • DOI: https://doi.org/10.1007/978-3-662-00932-1_3

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