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The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus

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Abstract

The evolutionary transition from water-breathing to air-breathing involved not only a change in function of the organs of respiratory gas exchange and N-waste excretion, but also in the organs of ion uptake from the environment. A combination of in vivo and in vitro techniques was used to look at the relative importance of the gills versus the gut in Na+, Cl−, and K+ balance in two closely related erythrinid species: a facultative air-breather, the jeju (Hoplerythrinus unitaeniatus) and an obligate water-breather, the traira (Hoplias malabaricus). The jeju has a well-vascularized physostomous swimbladder, while that in the traira is poorly vascularized, but the gills are much larger. Both species are native to the Amazon and are common in the ion-poor, acidic blackwaters of the Rio Negro. Under fasting conditions, the traira was able to maintain positive net Na+ and Cl− balance in this water, and only slightly negative net K+ balance. However, the jeju was in negative net balance for all three ions and had lower plasma Na+ and Cl− concentrations, despite exhibiting higher branchial Na+,K+ATPase and v-type H+ATPase activities. In the intestine, activities of these same enzymes were also higher in the jeju, and in vitro measurements of net area-specific rates of Na+, Cl−, and K+ absorption, as well as the overall intestinal absorption capacities for these three ions, were far greater than in the traira. When acutely exposed to disturbances in water O2 levels (severe hypoxia ~15 % or hyperoxia ~420 % saturation), gill ionoregulation was greatly perturbed in the traira but less affected in the jeju, which could “escape” the stressor by voluntarily air-breathing. We suggest that a shift of ionoregulatory capacity from the gills to the gut may have occurred in the evolutionary transition to air-breathing in jeju, and in consequence branchial ionoregulation, while less powerful, is also less impacted by variations in water O2 levels.

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Acknowledgments

Supported by FAPEAM and CNPq through the INCT-ADAPTA grant to ALV and VMFAV, a Ciência sem Fronteiras Grant to ALV and CMW, and an NSERC Discovery Grant to CMW. CMW is the recipient of a fellowship from the Ciência sem Fronteiras Program (CNPq-Brazil). ALV and VFAV are recipients of research fellowships from CNPq-Brazil. MG is supported by a Four Year Graduate Fellowship from the University of British Columbia. HSH was the recipient of a CNPq post-Doctoral fellowship from the Ciência sem Fronteiras Program. Special thanks to Gudrun De Boeck for the osmolality measurements, to Maria de Nazaré Paula da Silva, Sunita Nadella, and Ora Johannsson for assistance, and to two anonymous reviewers for constructive criticism.

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    Authors and Affiliations

    1. Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

      Chris M. Wood & Marina Giacomin

    2. Department of Biology, McMaster University, Hamilton, ON, Canada

      Chris M. Wood

    3. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Coral Gables, FL, USA

      Chris M. Wood

    4. Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil

      Chris M. Wood, Bernd Pelster, Marina Giacomin, Helen Sadauskas-Henrique, Vera Maria F. Almeida-Val & Adalberto Luis Val

    5. Institute of Zoology, University of Innsbruck, Innsbruck, Austria

      Bernd Pelster

    6. Center for Molecular Biosciences, University of Innsbruck, Innsbruck, Austria

      Bernd Pelster

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    1. Chris M. Wood
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    Correspondence to Chris M. Wood.

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    Communicated by G. Heldmaier.

    C. M. Wood and B. Pelster contributed equally to this paper.

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    Wood, C.M., Pelster, B., Giacomin, M. et al. The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus . J Comp Physiol B 186, 431–445 (2016). https://doi.org/10.1007/s00360-016-0965-5

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