Ablation of the ability to control the right-to-left cardiac shunt does not affect oxygen consumption, specific dynamic action or growth in rattlesnakes,Crotalus durissus

Abstract

SUMMARYThe morphologically undivided ventricle of the heart in non-crocodilian reptiles permits the mixing of oxygen-rich blood returning from the lungs and oxygen-poor blood from the systemic circulation. A possible functional significance for this intra-cardiac shunt has been debated for almost a century. Unilateral left vagotomy rendered the single effective pulmonary artery of the South American rattlesnake, Crotalus durissus, unable to adjust the magnitude of blood flow to the lung. The higher constant perfusion of the lung circulation and the incapability of adjusting the right-left shunt in left-denervated snakes persisted over time, providing a unique model for investigation of the long-term consequences of cardiac shunting in a squamate. Oxygen uptake recorded at rest and during spontaneous and forced activity was not affected by removing control of the cardiac shunt. Furthermore, metabolic rate and energetic balance during the post-prandial metabolic increment, plus the food conversion efficiency and growth rate, were all similarly unaffected. These results show that control of cardiac shunting is not associated with a clear functional advantage in adjusting metabolic rate, effectiveness of digestion or growth rates.Key words: cardiac shunt, vagotomy, rattlesnake, Crotalus, oxygen uptake, heart. THE JOURNAL OF EXPERIMENTAL BIOLOGY 1882 model to study the consequences of long-term manipulation of their ability to induce R-L cardiac shunts, we investigated the survivorship consequences of shunt ablation. This was achieved by measuring growth and food intake plus rates of oxygen uptake during rest, during spontaneous activity, following enforced activity and after ingestion of food in snakes vagotomised on the left or right side and in a control group subjected to a sham denervation. It has been argued that appetite, food conversion and long-term growth rate can provide more robust measures of fitness than measurement of physiological variables (Chamaille-Jammes et al., 2006;Eme et al., 2010;Sinervo and Adolph, 1989). MATERIALS AND METHODS Experimental animalsSouth American rattlesnakes [Crotalus durissus terrificus (Laurenti 1768)] used to study growth, food assimilation and metabolic rate, including specific dynamic action and activity, were born in captivity at the State University of São Paulo (UNESP) (Rio Claro, São Paulo State, Brazil). They were 1month old, with a mean mass of 30±4g (N=21) when the study commenced. An additional 16 adult snakes (1598±682g), acquired from the Butantan Institute (Sao Paulo) were used to determine oxygen uptake during rest and activity. The snakes were maintained individually in plastic boxes (40×29×27cm) at 28-30°C with ad libitum access to water. The snakes were fed to satiety on mice once a week, while the adult snakes were given rats to satiety every third week. Satiety was assumed when each snake stopped striking/ingesting the next in succession of the mice/rats offered. All experiments were approved by the ethical committee on animal experimentation (Comissã...

Loss of the Ability to Control Right-to-Left Shunt Does Not Influence the Metabolic Responses to Temperature Change or Long-Term Fasting in the South American RattlesnakeCrotalus durissus

“…Crotalus durissus spontaneously exhibits large R-L shunts when resting undisturbed, particularly at low body temperatures (Wang et al 1998;Taylor et al 2009;Leite et al 2013). The typical parasympathetic regulation of pulmonary blood flow in this species, however, differs from other noncrocodilian reptiles.…”

“…The experiments were performed on three groups of animals: sham-operated but otherwise intact (I) snakes and snakes with unilateral vagotomy on the left (LV) or on the right (RV) sides, as described by Leite et al (2013). For induction of anesthesia, each snake was placed in a closed plastic chamber and exposed to elevated levels of CO 2 until reflexes disappeared (see Wang et al 1993).…”

“…The nerve was sectioned unilaterally, with a 1-2-cm segment of nerve removed to reduce the possibility of nerve regeneration. Because the left vagus alone controls resistance in the pulmonary artery (Taylor et al 2009), the LV snakes were unable to control the cardiac shunt after prolonged recovery (Leite et al 2013). The RV group served as a control for any effect of unilateral vagotomy per se, while the sham-operated, intact group (I) served as a control for the operative procedures.…”

“…The RV group served as a control for any effect of unilateral vagotomy per se, while the sham-operated, intact group (I) served as a control for the operative procedures. The effectiveness and persistence of unilateral vagotomy were verified at the end of each experiment by recording the effect of peripheral stimulation of either vagus nerve (central to the point of transection) on heart rate and pulmonary and systemic blood flows (see Leite et al 2013). The hemodynamic effect of unilateral left vagotomy was shown to be persistent over time, allowing long-term experiments (Leite et al 2013).…”

“…Rattlesnakes, in common with some other species of snakes, possess a single functional lung. The single pulmonary artery is innervated by the left branch of the vagus nerve that acts to cause vasoconstriction, thus regulating pulmonary blood flow and consequent cardiac shunt patterns (Taylor et al 2009;Leite et al 2013). Sectioning the left vagus nerve causes an irreversible increase in pulmonary blood flow and prevents the generation of large R-L shunts while leaving intact parasympathetic innervation of other visceral organs, including the heart via the right vagus nerve (Taylor et al 2009;Leite et al 2013).…”