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

Abstract

Low O2 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.

Evidence for a carotid body homolog in the lizardTupinambis merianae

“…This suggests that muscarinic ACh receptors are involved in hypoxia chemoreception and, by extension, that ACh is an important neurotransmitter in the initiation of the cardiovascular response to hypoxemia. These results are supported by previous studies on turtles and rattlesnakes, which found that injection of atropine eliminated the tachycardia normally seen during hypoxia exposure (Comeau and Hicks, 1994;Skovgaard et al, 2005). Injection of methysergide also blocked the effect of NaCN on f H (Fig.…”

“…amphibians, birds and mammals) (Heistad and Abboud, 1980;Faraci, 1986;Kruhoffer et al, 1987;van Klaveren and Demedts, 1998;Andersen et al, 2003), stimulation of putative carotid artery chemoreceptors in lizards produced an increase in f H and f R while keeping MAP constant. The physical association of chemoreceptive cells in the carotid artery of the tegu, however, differed from the general pattern seen in most other terrestrial taxa.…”

“…The Journal of Experimental Biology (2015) doi:10.1242/jeb.111633 reducing inspired P O 2 resulted in a slight decrease in f H and an increase in ventilation exclusively through an increase in tidal volume (V T ), whereas f R remained unchanged (Skovgaard and Wang, 2004;Skovgaard et al, 2005).…”

“…The injections of NaCN used in the present study produced a localized, transient stimulus at a single chemoreceptive site. In the study of Skovgaard et al (Skovgaard et al, 2005), generalized hypoxia was sustained and would have acted at multiple chemoreceptive sites. Also, because of the design of our experiment, we could only measure changes in f R and not changes V T .…”

“…All drugs were purchased from Sigma-Aldrich. Concentrations considered safe for injection were determined from values reported previously (Kirby and Burnstock, 1969;Hohnke, 1975;Skovgaard et al, 2005).…”