Aquatic surface respiration, buoyancy control and the evolution of air-breathing in gobies (Gobiidae: Pisces)

The role of a buccal gas bubble, held while performing aquatic surface respiration (ASR; ventilating the gills with surface water during hypoxia), was examined in benthic, intertidal Australian gobies (Favonigobius tamarensis, F. exquisitus, Pseudogobius olorum, Chlamydogobius sp., Mugilogobius paludis, Cryptocentroides cristatus and Arenigobius bifrenatus). Analyses of the forces of lift and weight of the head and body during ASR indicate a hydrostatic role for the bubble. During ASR, lift from the bubble was sufficient to provide neutral or positive buoyancy to the head, anchoring the mouth at the water surface. A buoyancy role was confirmed by experiments demonstrating the ability of some species to alter bubble volume, to compensate either for different body positions or for water densities (salinities). Use of the bubble for aerial respiration by Cryptocentroides, Mugilogobius, Chlamydogobius and Arenigobius was confirmed in hypoxia by the presence of blood-filled capillaries in the buccal subepithelium (mean air­blood barrier less than 30 µm) in areas of the buccal cavity that contacted the bubble. Blood-filled capillaries were rare or absent in normoxia in all species except Mugilogobius. Cutaneous respiration was inferred from the presence of blood-filled capillaries in the dermis and epidermis of emersed portions of the head in Mugilogobius, Chlamydogobius and Arenigobius. The buccal bubble has respiratory and hydrostatic roles and there is support for the hypothesis that ASR and the buoyancy regulation (air-gulping) required to perform it effectively are prerequisite steps in the evolution of air-breathing in these gobies.