Repeated evolution of underwater rebreathing in diving Anolis lizards

Air-based respiration limits the use of aquatic environments by ancestrally terrestrial animals. To overcome this challenge, diving arthropods have evolved to respire without resurfacing using air held between their cuticle and surrounding water.(1-4) Inspired by natural history observations in Haiti (unpublished data) and Costa Rica,(5,6) we conducted experiments documenting routine air-based underwater respiration in several distantly related semi-aquatic Anolis lizard species. Semi-aquatic anoles live along neotropical streams and frequently dive for refuge or food,(7-12) remaining underwater for up to 18 min. While submerged, these lizards iteratively expire and re-inspire narial air bubbles-underwater rebreathing. Rebreathed air is used in respiration, as the partial pressure of oxygen in the bubbles decreases with experimental submersion time in living anoles, but not in mechanical controls. Non-aquatic anoles occasionally rebreathe when submerged but exhibit more rudimentary rebreathing behaviors. Anole rebreathing is facilitated by a thin air layer (i.e., a plastron, sensu Brocher(13)) supported by the animal's rugose skin upon submergence. Wesuggest that hydrophobic skin, which we observed in all sampled anoles,(14,15) may have been exaptative, facilitating the repeated evolution of specialized rebreathing in species that regularly dive. Phylogenetic analyses strongly suggest that specialized rebreathing is adaptive for semi-aquatic habitat specialists. Air-based rebreathing may enhance dive performance by incorporating dead space air from the buccal cavity or plastron into the lungs, facilitating clearance of carbon dioxide, or allowing uptake of oxygen from surrounding water (i.e., a physical gill mechanism(4,16)).

Automated summary

Diving arthropods and semi-aquatic anoles have evolved to respire underwater using air stored between their cuticle and surrounding water, allowing them to stay submerged for extended periods of time. This specialized adaptation, known as rebreathing, is facilitated by thin air layers supported by the animal's hydrophobic skin upon submergence, enhancing dive performance and enabling the clearance of carbon dioxide and uptake of oxygen from the surrounding water. The presence of this unique ability in semi-aquatic species suggests that specialized rebreathing is adaptive for habitat specialists in aquatic environments.