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. 2021 Nov;335(9-10):801-813.
doi: 10.1002/jez.2456. Epub 2021 Apr 5.

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

Andrea Y Frommel  1   2 , Garfield T Kwan  3 , Kaelan J Prime  3 , Martin Tresguerres  3 , Henrik Lauridsen  4 , Adalberto L Val  5 , Ligia U Gonçalves  5 , Colin J Brauner  1
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Changes in gill and air-breathing organ characteristics during the transition from water- to air-breathing in juvenile Arapaima gigas

Andrea Y Frommel et al. J Exp Zool A Ecol Integr Physiol. 2021 Nov.

Abstract

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.

Keywords: ATPase; Amazon fish; NKA; VHA; gill development; ionocytes; paiche; pirarucu; swim bladder.

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References

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