Changes in gill and air-breathing organ characteristics during the transition from water- to air-breathing in juvenile Arapaima gigas

The obligate air-breathing Amazonian fish, Arapaima gigas, hatch as water-breathing larvae but with development, they modify their swim bladder to an air-breathing organ (ABO) while reducing their gill filaments to avoid oxygen loss. Here, we show that significant changes already take place between 4 weeks (1.6 g) and 11 weeks (5 g) post hatch, with a reduction in gill lamellar surface area, increase in gill diffusion distance, and proliferation of the parenchyma in the ABO. By using a variety of methods, we quantified the surface area and diffusion distances of the gills and skin, and the swim bladder volume and anatomical complexity from hatch to 11-week-old juveniles. In addition, we identified the presence of two ionocyte types in the gills and show how these change with development. Until 1.6 g, A. gigas possess only the H+-excreting/Na+-absorbing type, while 5-g fish and adults have an additional ionocyte which likely absorbs H+ and Cl- and excretes HCO3-. The ionocyte density on the gill filaments increased with age and is likely a compensatory mechanism for maintaining ion transport while reducing gill surface area. In the transition from water- to air-breathing, A. gigas likely employs a trimodal respiration utilizing gills, skin, and ABO and thus avoid a respiratory-ion regulatory compromise at the gills.

Automated summary

The Amazonian fish, Arapaima gigas, undergo significant anatomical and physiological changes during development, transitioning from water-breathing larvae to air-breathing juveniles. These changes include reduction in gill surface area, increase in diffusion distance, and proliferation of ionocytes in the air-breathing organ. The fish utilize a trimodal respiration strategy involving gills, skin, and the air-breathing organ to maintain ion transport and avoid respiratory-ion regulatory compromise.