AERIAL RESPIRATION IN THE LONGJAW MUDSUCKER GILLICHTHYS MIRABILIS (TELEOSTEI: GOBIIDAE)

¹ Department of Biological Sciences, University of California, Santa Barbara, California

1. Like several other estuarine gobies, G. mirabilis, which ranges from central California through the Gulf of California, can breathe aerially by means of its heavily vascularized buccopharynx.

2. When environmental dissolved oxygen falls below 2.0 mg./l., the fish ceases all opercular movements during a preliminary period of adjustment, then gulps mouthfuls of air at the surface, usually retires to the bottom for a brief sojourn, and expels the respired air before the next gulp.

3. While gulping in the confinement of an inverted funnel, the fish consume oxygen and excrete carbon dioxide in almost direct proportion with the time that the gulped air bubble is held. The relatively low respiratory quotient (RQ) suggests that considerable carbon dioxide is excreted by the gills and, perhaps, skin, even when the fish is gulping. Respirometric measurements indicate rates of oxygen consumption to be similar for all active air-breathing mudsuckers, whether submergent and gulping or emergent and moist.

4. Its spacious buccopharynx is heavily vascularized, especially between the tongue and huccal roof, where the bubble is usually centered. The proliferation of capillaries in the buccopharyngeal epithelium simply represents an evolutionary expansion of homologous systems present in non-air-breathing relatives, rather than an evolutionary innovation. When fish are placed in water low in oxygen, histological changes are initiated which dilate the epithelial capillaries, engorging them with blood, and which corrugate, lubricate, and pit the epithelium, thereby creating a lung-like surface. Within a few minutes after transfer to deoxygenated water, the mouth is reddened by engorged vessels, although full functional adaptation is attained 10-20 minutes later when the fish begins gulping. An obligatory aquatic breather, Fundulus parvipinnis, exhibits no such changes.

5. Because during its pregulping period of adjustment the adult mudsucker ceases all opercular movements, an auxiliary oxygen store most likely supplies oxygen for continued aerobic metabolism. The obvious source in the swimbladder could sustain the fish at a standard rate for all or most of this period and, indeed, the percentage of oxygen here decreases by considerably more than half during this time. After being forcefully emptied, the swimbladder is refilled in 12 hours with gas of high oxygen and carbon dioxide concentrations, which decrease to normal after 48 hours. The relatively small swimbladder cannot create neutral buoyancy for the bottom-dwelling mudsucker unless it is augmented by the volume of an unusually large gulp of air.

6. Therefore, the mudsucker conforms to all necessary and sufficient criteria thus far investigated for air-breathing in fishes. Although relatively sluggish, the aquatic-breathing fish tolerates about the same low oxygen tensions as most other species.

7. The Gobiidae include several air-breathing species, among which the mudsucker is intermediate in specialization for aerial respiration between closely related but relatively unspecialized Quietula guaymasiae of the Gulf of California and semi-terrestrial Periophthalmus schlosseri of southeastern Asia. Its only congener, G. seta, resembles it in gulping habit, but exhibits several juvenile characteristics, such as its continuation of opercular movements while air-breathing.