Abstract
The undivided ventricle of non-crocodilian reptiles allows for intracardiac admixture of oxygen-poor and oxygen-rich blood returning via the atria from the systemic circuit and the lungs. The distribution of blood flow between the systemic and pulmonary circuits may vary, based on differences between systemic and pulmonary vascular conductances. The South American rattlesnake, Crotalus durissus, has a single pulmonary artery, innervated by the left vagus. Activity in this nerve controls pulmonary conductance so that left vagotomy abolishes this control. Experimental left vagotomy to abolish cardiac shunting had no effect on long-term survival and failed to identify a functional role in determining metabolic rate, growth or resistance to food deprivation. Accordingly, the present investigation sought to evaluate the extent to which cardiac shunt patterns are actively controlled during changes in body temperature and activity levels. We compared hemodynamic parameters between intact and left-vagotomized rattlesnakes held at different temperatures and subjected to enforced physical activity. Increased temperature and enforced activity raised heart rate, cardiac output, pulmonary and systemic blood flow in both groups, but net cardiac shunt was reversed in the vagotomized group at lower temperatures. We conclude that vagal control of pulmonary conductance is an active mechanism regulating cardiac shunts in C. durissus.
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Burggren WW (1977) The pulmonary circulation of the chelonian reptile: morphology, haemodynamics and pharmacology. J Comp Physiol B 116:303–323
Burggren WW (1978) Influence of intermittent breathing on ventricular depolarization patterns in chelonian reptiles. J Physiol 278:349–364
Burggren WW (1987) Form and function in reptilian circulations. Am Zool 27:5–19
Clark TD, Wang T, Butler PJ, Frappell PB (2005) Factorial scopes of cardio-metabolic variables remain constant with changes in body temperature in the varanid lizard, Varanus rosenbergi. Am J Physiol 288:R992–R997
Comeau SG, Hicks JW (1994) Regulation of central vascular blood flow in turtle. Am J Physiol 36:R569–R578
Crossley D, Altimiras J, Wang T (1998) Hypoxia elicits an increase in pulmonary vasculature resistance in anaesthetised turtles (Trachemys scripta). J Exp Biol 201:3367–3375
Crossley D, Wang T, Altimiras J (2000) Role of nitric oxide in the systemic and pulmonary circulation of anesthetized turtles (Trachemys scripta). J Exp Zool 286:683–689
Eme J, Gwalthney J, Blank JM, Owerkowicz T, Barron G, Hicks JW (2009) Surgical removal of right-to-left cardiac shunt in the American alligator (Alligator mississippiensis) causes ventricular enlargement but does not alter apnoea or metabolism during diving. J Exp Biol 212:3553–3563
Eme J, Gwalthney J, Owerkowicz T, Blank JM, Hicks JW (2010) Turning crocodilian hearts into bird hearts: growth rates are similar for alligators with and without right-to-left cardiac shunt. J Exp Biol 213:2673–2680
Filogonio R, Taylor EW, Carreira LBT, Leite GSPC, Abe AS, Leite CAC (2014) Systemic blood flow relations in conscious South American rattlesnakes. South Am J Herpetol 9:171–176
Frappell PB, Schultz T, 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
Galli G, Taylor EW, Wang T (2004) The cardiovascular responses of the freshwater turtle Trachemys scripta to warming and cooling. J Exp Biol 207:1471–1478
Galli G, Skovgaard N, Abe AS, Taylor EW, Wang T (2005a) The role of nitric oxide in the regulation of the systemic and pulmonary vasculature of the rattlesnake, Crotalus durissus terrificus. J Comp Physiol 175 B:201–208
Galli G, Skovgaard N, Abe AS, Taylor EW, Conlon JM, Wang T (2005b) Cardiovascular actions of rattlesnake bradykinin ([Val1, Thr6] bradykinin) in the anesthetized South American rattlesnake Crotalus durissus terrificus. Am J Physiol 288:R456–R465
Galli G, Skovgaard N, Abe AS, Taylor EW, Wang T (2007) The adrenergic regulation of the cardiovascular system in the South American rattlesnake, Crotalus durissus. Comp Biochem Phys 148 A:510–520
Gleeson TT, Mitchell GS, Bennett AF (1980) Cardiovascular responses to graded activity in the lizards Varanus and Iguana. Am J Physiol 239:R174–R179
Goodman LA (1969) On the exact variance of products. J Am Stat Assoc 55:708–713
Herman JK, Smatresk NJ (1999) Cardiorespiratory response to progressive hypoxia and hypercapnia in the turtle Trachemys scripta. J Exp Biol 202:3205–3213
Hicks JW (1994) Adrenergic and cholinergic regulation of intracardiac shunting. Physiol Zool 67:1325–1346
Hicks JW (2002) The evolutionary and physiological significance of cardiovascular shunting patterns in reptiles. News Physiol Sci 17:241–245
Hicks JW, Comeau SG (1994) Vagal regulation of intracardiac shunting in the turtle Pseudemys scripta. J Exp Biol 186:109–126
Hicks JW, Krosniunas E (1996) Physiological states and intracardiac shunting in non-crocodilian reptiles. Exp Biol Online 1:35–57
Hicks JW, Wang T (2012) The functional significance of the reptilian heart: new insights into an old question. In: Wang T, Sedmera D (eds) Ontogeny and phylogeny of the heart. Springer, New York, pp 207–227
Hicks JW, Ishimatsu A, Molli S, Erskin A, Heisler N (1996) The mechanism of cardiac shunting in reptiles: a new synthesis. J Exp Biol 199:1435–1446
Hillman SS, Hedrick MS, Kohl ZF (2014) Net cardiac shunts in anuran amphibians: physiology or physics? J Exp Biol 217:2844–2847
Jensen B, Abe AS, Andrade DV, Nyengaard JR, Wang T (2010) The heart of the South American rattlesnake, Crotalus durissus. J Morphol 271:1066–1077
Joyce W, Wang T (2014) Adenosinergic regulation of the cardiovascular system in the red-eared slider Trachemys scripta. Comp Biochem Physiol 174 A:18–22
Kempen GMP, Vliet LJ (2000) Mean and variance of ratio estimators used on fluorescence ratio imaging. Cytometry 39:300–305
Kinney JL, Matsuura DT, White FN (1977) Cardiorespiratory effects of temperature in the turtle, Pseudemys floridana. Respir Physiol 31:309–325
Kohl ZF, Hedrick MS, Hillman SS (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 183 B:921–932
Krosniunas EH, Hicks JW (2003) Cardiac output and shunt during voluntary activity at different temperatures in the turtle, Trachemys scripta. Physiol Biochem Zool 76:679–694
Leite CAC, Taylor EW, Wang T, Abe AS, Andrade DOV (2013) Ablation of the ability to control the right-to-left cardiac shunt does not affect oxygen uptake, specific dynamic action or growth in the rattlesnake Crotalus durissus. J Exp Biol 216:1881–1889
Leite CAC, Wang T, Taylor EW, Abe AS, Leite GSPC, Andrade DOV (2014) Loss of the ability to control R–L shunt does not influence the metabolic responses to temperature change or long-term fasting in the South American rattlesnake, Crotalus durissus. Physiol Biochem Zool 87:568–575
Lillywhite HB, Zippel KC, Farrell AP (1999) Resting and maximal heart rates in ectothermic vertebrates. Comp Biochem Phys 124 A:369–382
Luckhardt AB, Carlson AJ (1921) Studies on the visceral sensory nervous system. VIII. On the presence of vasomotor fibers in the vagus nerve to the pulmonary vessels of the amphibian and the reptilian lung. Am J Physiol 56:72–112
Milsom WK, Langille BL, Jones DR (1977) Vagal control of pulmonary vascular resistance in the turtle Chrysemys scripta. Can J Zool 55:359–367
Seebacher F (2009) Responses to temperature variation: integration of thermoregulation and metabolism in vertebrates. J Exp Biol 212:2885–2891
Stecyk JAW, Overgaard J, Farrell AP, Wang T (2004) α-Adrenergic regulation of systemic peripheral resistance and blood flow distribution in the turtle Trachemys scripta during anoxic submergence at 5 °C and 21 °C. J Exp Biol 207:269–283
Stinner JN (1987) Cardiovascular and metabolic responses to temperature in Coluber constrictor. Am J Physiol 253:R222–R227
Taylor EW, Andrade DV, Abe AS, Leite CAC, Wang T (2009) The unequal influences of the left and right vagi on the control of the heart and pulmonary artery in the rattlesnake, Crotalus durissus. J Exp Biol 212:145–151
Tucker VA (1966) Oxygen transport by the circulatory system of the green iguana (Iguana iguana) at different body temperatures. J Exp Biol 44:77–92
Wang T, Hicks JW (1996a) The interaction of pulmonary ventilation and the right-left shunt on arterial oxygen levels. J Exp Biol 199:2121–2129
Wang T, Hicks JW (1996b) Cardiorespiratory synchrony in turtles. J Exp Biol 199:1791–1800
Wang T, Hicks JW (2008) Changes in pulmonary blood flow do not affect gas exchange during intermittent ventilation in resting turtles. J Exp Biol 211:3759–3763
Wang T, Fernandes W, Abe AS (1993) Blood pH and O2 homeostasis upon CO2 anesthesia in the rattlesnake (Crotalus durissus). Snake 25:21–26
Wang T, Krosniunas E, Hicks JW (1997) The role of cardiac shunts in the regulation of arterial blood gases. Am Zool 37:12–22
Wang T, Abe AS, Glass ML (1998) Effects of temperature on lung and blood gases in the South American rattlesnake Crotalus durissus terrificus. Comp Biochem Phys 121 A:7–11
Wang T, Warburton S, Abe AS, Taylor EW (2001) Vagal control of heart rate and cardiac shunts in reptiles: relation to metabolic state. Exp Physiol 86:777–784
West NH, Butler PJ, Bevan RM (1992) Pulmonary blood flow at rest and during swimming in the green turtle, Chelonia mydas. Physiol Zool 65:287–310
Wood SC, Johansen K, Gatz RN (1977) Pulmonary blood flow, ventilation/perfusion ratio, and oxygen transport in a varanid lizard. Am J Physiol 2:R89–R93
Acknowledgments
We thank the Butantan Institute for providing, and Carlinhos and Joniel for taking care of snakes used in this study; R Labouriau and JR Knaub for statistical help; JE Carvalho and LH Florindo for valued comments on previous versions of the manuscript. PB Dickinson, JM Osbourne and J Petrucci were great motivators throughout the study. This study was funded by the Fundação de Amparo à pesquisa do Estado de São Paulo and Conselho Nacional de Desenvolvimento Científico e Tecnológico through the Instituto Nacional de Ciência e Tecnologia em Fisiologia Comparada. RF received a stipend from Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior through the Ciência sem Fronteiras programme, CACL had financial support from FAPESP, ASA from CNPq, EWT was supported both by FAPESP and by CNPq through the Ciência sem Fronteiras programme and TW was supported by the Danish Research Council.
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Communicated by H. V. Carey.
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Filogonio, R., Wang, T., Taylor, E.W. et al. Vagal tone regulates cardiac shunts during activity and at low temperatures in the South American rattlesnake, Crotalus durissus . J Comp Physiol B 186, 1059–1066 (2016). https://doi.org/10.1007/s00360-016-1008-y
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DOI: https://doi.org/10.1007/s00360-016-1008-y