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First published online March 22, 2004
Journal of Experimental Biology 207, 1433-1438 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00887

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Commentary

Transition in organ function during the evolution of air-breathing; insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon

C. J. Brauner^1,*, V. Matey², J. M. Wilson³, N. J. Bernier⁴ and A. L. Val⁵

¹ Department of Zoology, University of British Columbia, 6270 University Blvd, Vancouver, BC, Canada, V6T 1Z4,
² Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182, USA,
³ Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Rua dos Bragas 177, 4050-123 Porto, Portugal,
⁴ Department of Zoology, University of Guelph, Guelph, ON, Canada, N1G 2W1
⁵ National Institute for Research in the Amazon (INPA), Laboratory of Ecophysiology and Molecular Evolution, Ave André Araújo 2936, CEP 69083-000, Manaus, AM, Brazil

^* Author for correspondence (e-mail: brauner{at}zoology.ubc.ca)

Accepted 19 January 2004

The transition from aquatic to aerial respiration is associated with dramatic physiological changes in relation to gas exchange, ion regulation, acid–base balance and nitrogenous waste excretion. Arapaima gigas is one of the most obligate extant air-breathing fishes, representing a remarkable model system to investigate (1) how the transition from aquatic to aerial respiration affects gill design and (2) the relocation of physiological processes from the gills to the kidney during the evolution of air-breathing. Arapaima gigas undergoes a transition from water- to air-breathing during development, resulting in striking changes in gill morphology. In small fish (10 g), the gills are qualitatively similar in appearance to another closely related water-breathing fish (Osteoglossum bicirrhosum); however, as fish grow (100–1000 g), the inter-lamellar spaces become filled with cells, including mitochondria-rich (MR) cells, leaving only column-shaped filaments. At this stage, there is a high density of MR cells and strong immunolocalization of Na⁺/K⁺-ATPase along the outer cell layer of the gill filament. Despite the greatly reduced overall gill surface area, which is typical of obligate air-breathing fish, the gills may remain an important site for ionoregulation and acid–base regulation. The kidney is greatly enlarged in A. gigas relative to that in O. bicirrhosum and may comprise a significant pathway for nitrogenous waste excretion. Quantification of the physiological role of the gill and the kidney in A. gigas during development and in adults will yield important insights into developmental physiology and the evolution of air-breathing.

Key words: air-breathing, gills, kidney, Arapaima gigas, Osteoglossum bicirrhosum, gas exchange, ionoregulation, acid–base balance, nitrogenous waste excretion

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