Respiratory Control in the Transition from Water to Air Breathing in Vertebrates

Abstract

SYNOPSIS. Studies on extant bimodally breathing vertebrates offer us a chance to gain insight into the changes in respiratory control during the evolutionary transition from water to air breathing. In primitive Actinopterygian air-breathingfishes (Lepisosteus and Amid) , gill ventilation is driven by an endogenously active central rhythm generator that is powerfully modulated by afferent input from internally and externally oriented branchial chemoreceptors, as it is in water-breathing Actinopterygians. The effects of internal or external chemoreceptor stimulation on water and air breathing vary substantially in these aquatic air breathers, suggesting that their roles are evolutionarily malleable. Air breathing in these bimodal breathers usually occurs as single breaths taken at irregular intervals and is an on-demand phenomenon activated primarily by afferent input from the branchial chemoreceptors. There is no evidence for central CO2/pH sensitive chemoreceptors and air-breathing organ mechanoreceptors have little influence over branchial- or air-breathing patterns in Actinopterygian air breathers. In the Sarcopterygian lungfish Lepidosiren and Protopterus , ventilation of the highly reduced gills is relatively unresponsive to chemoreceptor or mechanoreceptor input. The branchial chemoreceptors of the anterior arches appear to monitor arterialized blood, while chemoreceptors in the posterior arches may monitor venous blood. Lungfish respond vigorously to hypercapnia, but it is not known whether these responses are mediated by central or peripheral chemoreceptors. A major difference between the Sarcopterygian and Actinopterygian bimodal breathers is that lungfish can inflate their lungs using rhythmic bouts of air breathing, and lung mechanoreceptors influence the onset and termination of these lung inflation cycles. The control of breathing in amphibians appears similar to that of lungfish. Branchial ventilation may persist as rhythmic buccal oscillations in most adults, and stimulation of peripheral chemoreceptors in the aortic arch or carotid labyrinths initiates short bouts of breathing. Ventilation is much more responsive to hypercapnia in adult amphibians than in Actinopterygian fishes because of central CO2/pH sensitive chemoreceptors that act to convert periodic to more continuous breathing patterns when stimulated.