The highly specialized secretory epithelium in the buccal cavity of the alkalinity adapted Lake Magadi cichlid, Oreochromis alcalicus grahami (Teleostei: Cichlidae): a scanning and transmission electron microscope study

Abstract

Oreochromis alcalicus grahami is a small cichlid fish that lives in the hot, highly alkaline, highly saline peripheral lagoons of Lake Magadi, Kenya. The fish faces profound diurnal oscillations of oxygen concentration. During the day, from photosynthetic activity of cyanobacteria (blue-green algae), the water is supersaturated with oxygen but after sunset when photosynthetic activity stops the water is virtually anoxic as a result of bacterial respiration. During the night and after explosive exercise, O. a. grahami characteristically skims the surface of the water with the mouth agape, suggesting that the buccal cavity is used as a gas-exchange organ. Contrary to expectation, however, the buccal cavity was found to be conspicuously non-vascularized: the surface epithelial lining was fundamentally of a mucus secretory type. In addition, certain cells in the deeper layers showed extensive lateral labyrinths similar to the epithelium of the renal tubules. These morphological features respectively indicated roles of secreting a protective film and regulation of ions taken across the epithelial lining of the buccal cavity. The allocation of gas-exchange to the gills and the air-bladder, osmoregulation essentially to the gills, and mucus secretion/protection to the buccal cavity displays an adaptive trade-off process in an elite animal. Effective use of the buccal cavity as a gas-exchanger would entail air-gulping followed by brief retention of it in the cavity to allow oxygen uptake. During such interval, both the gills and the air-bladder would of necessity be rendered temporarily non-functional. Skimming the top layer of water with the mouth open ensures that the gills are passively ventilated with well aerated water and the air-bladder is simultaneously used for gas-exchange, a strategy that should enhance oxygen acquisition, especially at higher ambient temperatures.