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

SYNOPSIS. Studies on extant bimodally breathing vertebratesoffer us a chance to gain insight into the changes in respiratorycontrol during the evolutionary transition from water to airbreathing. In primitive Actinopterygian air-breathingfishes(Lepisosteus and Amid), gill ventilation is driven by an endogenouslyactive central rhythm generator that is powerfully modulatedby afferent input from internally and externally oriented branchialchemoreceptors, as it is in water-breathing Actinopterygians.The effects of internal or external chemoreceptor stimulationon water and air breathing vary substantially in these aquaticair breathers, suggesting that their roles are evolutionarilymalleable. Air breathing in these bimodal breathers usuallyoccurs as single breaths taken at irregular intervals and isan on-demand phenomenon activated primarily by afferent inputfrom the branchial chemoreceptors. There is no evidence forcentral CO₂/pH sensitive chemoreceptors and air-breathing organmechanoreceptors have little influence over branchial- or air-breathingpatterns in Actinopterygian air breathers. In the Sarcopterygianlungfish Lepidosiren and Protopterus, ventilation of the highlyreduced gills is relatively unresponsive to chemoreceptor ormechanoreceptor input. The branchial chemoreceptors of the anteriorarches appear to monitor arterialized blood, while chemoreceptorsin the posterior arches may monitor venous blood. Lungfish respondvigorously to hypercapnia, but it is not known whether theseresponses are mediated by central or peripheral chemoreceptors.A major difference between the Sarcopterygian and Actinopterygianbimodal breathers is that lungfish can inflate their lungs usingrhythmic bouts of air breathing, and lung mechanoreceptors influencethe onset and termination of these lung inflation cycles. Thecontrol of breathing in amphibians appears similar to that oflungfish. Branchial ventilation may persist as rhythmic buccaloscillations in most adults, and stimulation of peripheral chemoreceptorsin the aortic arch or carotid labyrinths initiates short boutsof breathing. Ventilation is much more responsive to hypercapniain adult amphibians than in Actinopterygian fishes because ofcentral CO₂/pH sensitive chemoreceptors that act to convertperiodic to more continuous breathing patterns when stimulated.