Changes in gill and air‐breathing organ characteristics during the transition from water‐ to air‐breathing in juvenile Arapaima gigas. Issue 9 (5th April 2021)

• Record Type: Journal Article
• Authors: Frommel, Andrea Y.; Kwan, Garfield T.; Prime, Kaelan J.; Tresguerres, Martin; Lauridsen, Henrik; Val, Adalberto L.; Gonçalves, Ligia U.; Brauner, Colin J.
• Other Names: Pelster Bernd guestEditor.; Val Adalberto L. guestEditor.
• Is Part Of: Journal of experimental zoology. Volume 335:Issue 9/10(2021)
• Page Start: 801
• Page End: 813
• Publication Date: 2021-04-05
• Subjects: Amazon fish -- ATPase -- gill development -- ionocytes -- NKA -- paiche -- pirarucu -- swim bladder -- VHA; Zoology -- Periodicals; Zoology; Animal Population Groups -- physiology; Zoology; Electronic journals; Periodical; Periodicals; 590
• DOI: 10.1002/jez.2456
• Languages: English
• ISSNs: 2471-5646

Abstract

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. Abstract : Remodeling of respiratory compartments in juvenile Arapaima gigas developing in oxygen‐ and ion‐poor waters of the Amazon River. Highlights: Significant transformations in gill, skin, and ABO between 1.6 and 5.5 g body mass of A. gigas with the transition from water‐ to air breathing Larval A. gigas gills have one ionocyte type for Na + and H + regulation, while older juveniles and adults have an additional ionocyte type for Cl − and HCO3 −