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Gill paracellular permeability and the osmorespiratory compromise during exercise in the hypoxia-tolerant Amazonian oscar (Astronotus ocellatus)

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Abstract

In the traditional osmorespiratory compromise, fish increase their effective gill permeability to O2 during exercise or hypoxia, and in consequence suffer unfavorable ionic and osmotic fluxes. However oscars, which live in the frequently hypoxic ion-poor waters of the Amazon, actually decrease ionic fluxes across the gills during acute hypoxia without changing gill paracellular permeability, and exhibit rapid paving over of the mitochondrial-rich cells (MRCs). But what happens during prolonged exercise? Gill paracellular permeability, ionic fluxes, and gill morphology were examined in juvenile oscars at rest and during aerobic swimming. Initial validation tests with urinary catheterized fish quantified drinking, glomerular filtration, and urinary flow rates, and confirmed that measurements of gill paracellular permeability as [3H]PEG-4000 clearances were the same in efflux and influx directions, but far lower than previously measured in comparably sized trout. Although the oscars achieved a very similar proportional increase (90 %) in oxygen consumption (MO2) to trout during steady-state swimming at 1.2 body lengths sec−1, there was no increase in gill paracellular permeability, in contrast to trout. However, oscars did exhibit increased unidirectional Na+ efflux and net K+ rates during exercise, but no change in drinking rate. There were no changes in MRC numbers or exposure, or other alterations in gill morphology during exercise. A substantial interlamellar cell mass (ILCM) that covered the lamellae to a depth of 30 % was unchanged by 4 h of swimming activity. We conclude that a low branchial paracellular permeability which can be dissociated from changes in O2 flux, as well as the presence of the ILCM, may be adaptive in limiting ionoregulatory costs for a species endemic to ion-poor, frequently hypoxic waters.

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Acknowledgments

Supported in Manaus, Brazil by FAPEAM and CNPq through the INCT-ADAPTA grant to ALV, and Ciência sem Fronteiras grant to ALV and CMW, in Rio Grande, Brazil by an award from the International Development Research Centre (IDRC) and the Canada Research Chair Program to AB and CMW, and an award from CNPq to AB in the scope of INCT-TA, and in Canada by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to CMW. LMR was supported by an Ontario Graduate Scholarship. DK was a recipient of a PhD fellowship from CNPq. CMW was supported by the Canada Research Chairs program, and is the recipient of a fellowship from the Science Without Borders Program (CNPq-Brazil). ALV, VFAV, and AB are recipients of research fellowships from CNPq, and AB is also supported by the International Research Chair Program of IDRC. We thank two anonymous reviewers for constructive comments.

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Authors and Affiliations

  1. Department of Biology, McMaster University, Hamilton, ON, L8S 4K1, Canada

    Lisa M. Robertson & Chris M. Wood

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

    Daiani Kochhann, Vera F. Almeida-Val & Adalberto Luis Val

  3. Universidade Federal do Rio Grande (FURG), Rio Grande, RS, Brazil

    Adalto Bianchini

  4. Department of Biology, San Diego State University, San Diego, CA, 92182, USA

    Victoria Matey

  5. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, 33149, USA

    Chris M. Wood

  6. Department of Zoology, University of British Columbia, 4200 University Boulevard, Vancouver, BC, V6T 1Z4, Canada

    Chris M. Wood

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  1. Lisa M. Robertson
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Correspondence to Chris M. Wood.

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Communicated by G. Heldmaier.

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Robertson, L.M., Kochhann, D., Bianchini, A. et al. Gill paracellular permeability and the osmorespiratory compromise during exercise in the hypoxia-tolerant Amazonian oscar (Astronotus ocellatus). J Comp Physiol B 185, 741–754 (2015). https://doi.org/10.1007/s00360-015-0918-4

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