The role of nitric oxide in regulation of the cardiovascular system in reptiles

The roles that nitric oxide (NO) plays in the cardiovascular system of reptiles are reviewed, with particular emphasis on its effects on central vascular blood flows in the systemic and pulmonary circulations. New data is presented that describes the effects on hemodynamic variables in varanid lizards of exogenously administered NO via the nitric oxide donor sodium nitroprusside (SNP) and, preliminary data on the effects of SNP inhibition of nitric oxide synthase (NOS) by L-nitroarginine methyl ester (L-NAME). Furthermore. on hemodynamic variables in the tegu lizard are presented. The findings are compared with previously published data from Our laboratory on three other species of reptiles: pythons (Skovgaard, N., Galli, G., Taylor, E.W., Conlon, J.M., Wang.. T., 2005. Hemodynamic effects of python neuropeptide gamma in the anesthetized python, Python regius. Regul. Pept. 18, 15-26), rattlesnakes (Galli, G., Skovgaard, N., Abe, A.S., Taylor, E.W., Wang, T., 2005. The role of nitric oxide in the regulation of the systemic and the pulmonary vasculature of the rattlesnake, Crotalus durissus terrificus. J. Comp. Physiol. 175B, 201-208) and turtles (Crossley, D.A., 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). These five species of reptiles possess different combinations of division of the heart and structural complexity of the lungs. Comparison of their responses to NO donors and NOS inhibitors may reveal whether the potential contribution of NO to vascular tone correlates with pulmonary complexity and/or with blood pressure. All existing studies oil reptiles have clearly established a potential role for NO in regulating vascular tone in the systemic circulation and NO may be important for maintaining basal systemic vascular tone in varanid lizards, pythons and turtles, through a continuous release of NO. In contrast., the pulmonary circulation is less responsive to NO donors or NOS inhibitors, and it was only in pythons and varanid lizards that the lungs responded to SNP. Both species have a functionally separated heart, so it is possible that NO may exert a larger role in species with low pulmonary blood pressures, irrespective of lung complexity. (C) 2005 Elsevier B.V. All rights reserved.

Diet of the rattlesnake Crotalus durissus in southeastern Brazil (Serpentes, Viperidae)

Gut contents of 633 live rattlesnakes from southeastern Brazil received at the Instituto Butantanitute, SP, Brazil between 1993 and 1995 were studied. The snakes were weighed, measured and sexed. Two hundred and fifty-nine rattlesnakes had stomach and/or intestinal contents. Prey size was estimated by comparison of prey items with specimens from museum collections. Rodents and small marsupials were the main prey eaten by the rattlesnakes, and only 1% of the items were found in the stomach, whereas 41% of the individuals in the sample had feces in the intestine. There was low correlation between size of snake and prey size. No seasonal difference in frequency was found between fed and not fed males, but the occurrence of fed females was significantly lower during summer than winter months (28.9% and 51.8%, respectively). Fed newborn rattlesnakes had the lowest frequency, and also fed on rodents.

Arterial acid-base status during digestion and following vascular infusion of NaHCO3 and HCl in the South American rattlesnake, Crotalus durissus

Digestion is associated with gastric secretion that leads to an alkalinisation of the blood, termed the alkaline tide. Numerous studies on different reptiles and amphibians show that while plasma bicarbonate concentration ([HCO3-](pl)) increases substantially during digestion, arterial pH (pHa) remains virtually unchanged, due to a concurrent rise in arterial PCO2 (PaCO2) caused by a relative hypoventilation. This has led to the suggestion that postprandial amphibians and reptiles regulate pHa rather than PaCO2.Here we characterize blood gases in the South American rattlesnake (Crotalus durissus) during digestion and following systemic infusions of NaHCO3 and HCl in fasting animals to induce a metabolic alkalosis or acidosis in fasting animals. The magnitude of these acid-base disturbances were similar in magnitude to that mediated by digestion and exercise. Plasma [HCOT] increased from 18.4+/-1.5 to 23.7+/-1.0 mmol L-1 during digestion and was accompanied by a respiratory compensation where PaCO2 increased from 13.0+/-0.7 to 19.1+/-1.4 mm Hg at 24 h. As a result, pHa decreased slightly, but were significantly below fasting levels 36 h into digestion. Infusion of NaHCO3 (7 mmol kg(-1)) resulted in a 10 mmol L-1 increase in plasma [HCO3-] within 1 h and was accompanied by a rapid elevation of pHa (from 7.58+/-0.01 to 7.78+/-0.02). PaCO2, however, did not change following HCO3- infusion, which indicates a lack of respiratory compensation. Following infusion of HCl (4 mmol kg(-1)), plasma pHa decreased by 0.07 units and [HCO3-](pl) was reduced by 4.6 mmol L-1 within the first 3 h. PaCO2, however, was not affected and there was no evidence for respiratory compensation.Our data show that digesting rattlesnakes exhibit respiratory compensations to the alkaline tide, whereas artificially induced metabolic acid-base disturbances of same magnitude remain uncompensated. It seems difficult to envision that the central and peripheral chemoreceptors would experience different stimuli during these conditions. One explanation for the different ventilatory responses could be that digestion induces a more relaxed state with low responsiveness to ventilatory stimuli. (C) 2005 Elsevier B.V. All rights reserved.

The unequal influences of the left and right vagi on the control of the heart and pulmonary artery in the rattlesnake, Crotalus durissus

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Physiological importance of the coronary arterial blood supply to the rattlesnake heart

The reptilian heart consists of a thick inner spongy myocardium that derives its oxygen and nutrient supply directly from the blood within the ventricular cavity, which is surrounded by a thin outer compact layer supplied by coronary arteries. The functional importance of these coronary arteries remains unknown. In the present study we investigate the effects of permanent coronary artery occlusion in the South American rattlesnake (Crotalus durissus) on the ability to maintain heart rate and blood pressure at rest and during short term activity. We used colored silicone rubber (Microfil) to identify the coronary artery distribution and interarterial anastomoses. The coronary circulation was occluded and the snakes were then kept for 4 days at 30 degrees C. Microfil injections verified that virtually all coronary arteries had successfully been occluded, but also made visible an extensive coronary supply to the outer compact layer in untreated snakes. Electrocardiogram (ECG), blood pressure (P(sys)) and heart rate (f(H)) were measured at rest and during enforced activity at day 1 and 4. Four days after occlusion of the coronary circulation, the snakes could still maintain a P(sys) and f(H) of 5.2 +/- 0.2 kPa and 58.2 +/- 2.2 beats min(-1), respectively, during activity and the ECG was not affected. This was not different from sham-operated snakes. Thus, while the outer compact layer of the rattlesnake heart clearly has an extensive coronary supply, rattlesnakes sustain a high blood pressure and heart rate during activity without coronary artery blood supply.

Microhabitat use by species of the genera Bothrops and Crotalus (Viperidae) in semi-extensive captivity

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Hypoxic pulmonary vasoconstriction in reptiles: a comparative study of four species with different lung structures and pulmonary blood pressures

Low O-2 levels in the lungs of birds and mammals cause constriction of the pulmonary vasculature that elevates resistance to pulmonary blood flow and increases pulmonary blood pressure. This hypoxic pulmonary vasoconstriction (HPV) diverts pulmonary blood flow from poorly ventilated and hypoxic areas of the lung to more well-ventilated parts and is considered important for the local matching of ventilation to blood perfusion. In the present study, the effects of acute hypoxia on pulmonary and systemic blood flows and pressures were measured in four species of anesthetized reptiles with diverse lung structures and heart morphologies: varanid lizards (Varanus exanthematicus), caimans (Caiman latirostris), rattlesnakes (Crotalus durissus), and tegu lizards (Tupinambis merianae). As previously shown in turtles, hypoxia causes a reversible constriction of the pulmonary vasculature in varanids and caimans, decreasing pulmonary vascular conductance by 37 and 31%, respectively. These three species possess complex multicameral lungs, and it is likely that HPV would aid to secure ventilation-perfusion homogeneity. There was no HPV in rattlesnakes, which have structurally simple lungs where local ventilation-perfusion inhomogeneities are less likely to occur. However, tegu lizards, which also have simple unicameral lungs, did exhibit HPV, decreasing pulmonary vascular conductance by 32%, albeit at a lower threshold than varanids and caimans (6.2 kPa oxygen in inspired air vs. 8.2 and 13.9 kPa, respectively). Although these observations suggest that HPV is more pronounced in species with complex lungs and functionally divided hearts, it is also clear that other components are involved.

Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Caracaterização ultrassonográfica, morfofisiológica do sistema reprodutor de machos e fêmeas de Crotalus durissus terrificus

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Influência do controle vagal na resistência vascular pulmonar e desvio intracardíaco em Crotalus durissus (Squamata: Viperidae)

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

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 Rattlesnake Crotalus durissus

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Does the rattle of Crotalus durissus terrificus reveal its dietary history?

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Influência da temperatura e do termoperíodo sobre a taxa metabólica de repouso em cascavéis, Crotalus durissus (Serpentes: Viperidae)

Snakes are ectothermic animals and, therefore, their physiological functions are strongly affected by temperature. For instance, the resting metabolic rate (RMR) of this animals increase with the rise in body temperature. However, metabolic determinations in ectothermic organisms, including snakes, are generally made by submitting the animals to constant temperature regimes. This experimental procedure, although widely used, accepted and certainly suitable in several cases, submit the animals to a very different situation from that experienced by them in nature. In fact, ectothermics are known by presenting extensive variations in their body temperatures trough the day and/or seasons. If this disagreement between the thermal biology of the animals and the experimental conditions, for instance over the circadian cycle, affects the determinations of metabolic rates of ectotherm animals, remains quite uncertain. Thus, this study aimed to test the effects of different thermal regimes (fluctuating vs constant) in different temperature ranges over the TMR of rattlesnakes (Crotalus durissus). Therefore, the TMR of rattlesnakes was measured by the oxygen consumption rates ( V O2) in the constant temperatures of 15°C, 20°C, 25°C, 30°C and 35°C. For fluctuating regimes, snakes were measured in thermoperiods of 12/12 hours, as follows: 15°C and 25°C; 20°C and 30°C; 25°C and 35°C. Our results show that the RMR of C. durissus rises as the temperature increases, regardless of the thermal regime. The obtained RMR in the constant regimes of 20°C and 25°C was not different from that measured in the correspondent fluctuating regimes (i.e., 15 - 25°C e 20 - 30°C). However, at constant 30°C, the RMR was significantly higher than that obtained in the 30°C fluctuating regime (25 - 35ºC). This indicates that the potential effects in submitting of snakes to different thermal regimes of its thermal biology become more important with...

Influência da temperatura e do termoperíodo sobre a taxa metabólica de repouso em cascavéis, Crotalus durissus (Serpentes: Viperidae)

Snakes are ectothermic animals and, therefore, their physiological functions are strongly affected by temperature. For instance, the resting metabolic rate (RMR) of this animals increase with the rise in body temperature. However, metabolic determinations in ectothermic organisms, including snakes, are generally made by submitting the animals to constant temperature regimes. This experimental procedure, although widely used, accepted and certainly suitable in several cases, submit the animals to a very different situation from that experienced by them in nature. In fact, ectothermics are known by presenting extensive variations in their body temperatures trough the day and/or seasons. If this disagreement between the thermal biology of the animals and the experimental conditions, for instance over the circadian cycle, affects the determinations of metabolic rates of ectotherm animals, remains quite uncertain. Thus, this study aimed to test the effects of different thermal regimes (fluctuating vs constant) in different temperature ranges over the TMR of rattlesnakes (Crotalus durissus). Therefore, the TMR of rattlesnakes was measured by the oxygen consumption rates ( V O2) in the constant temperatures of 15°C, 20°C, 25°C, 30°C and 35°C. For fluctuating regimes, snakes were measured in thermoperiods of 12/12 hours, as follows: 15°C and 25°C; 20°C and 30°C; 25°C and 35°C. Our results show that the RMR of C. durissus rises as the temperature increases, regardless of the thermal regime. The obtained RMR in the constant regimes of 20°C and 25°C was not different from that measured in the correspondent fluctuating regimes (i.e., 15 - 25°C e 20 - 30°C). However, at constant 30°C, the RMR was significantly higher than that obtained in the 30°C fluctuating regime (25 - 35ºC). This indicates that the potential effects in submitting of snakes to different thermal regimes of its thermal biology become more important with...

JUVENILE RECRUITMENT, EARLY GROWTH, AND MORPHOLOGICAL VARIATION IN THE ENDANGERED SANTA CATALINA ISLAND RATTLESNAKE, CROTALUS CATALINENSIS

Life-history information constitutes the raw data for building population models used in species conservation. We provide life-history data for the endangered Santa Catalina Island Rattlesnake, Crotalus catalinensis. We use data from 277 observations of C. catalinensis made between 2002 and 2011 on the island. Mean snout-vent length (SVL) of adult C. catalinensis was 643 mm for males and 631 mm for females; the difference was not significant. The degree of sexual size dimorphism (SSD; using SVL) was -0.02. However, sexes were dimorphic in total length ( SVL + tail length), relative tail length, and stoutness. Juvenile recruitment occurs during late-summer. In their first year of life, juveniles seem to grow at a rate of about 1.7 cm/mo. Females seem to become mature around 570 mm SVL, probably in the year when they become 2 y old. Scattered literature data corroborates the time of juvenile recruitment described herein. Growth in C. catalinensis seems to be slower than that of C. ruber, its sister taxa, but similar to other rattlesnakes.