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Air breathing and aquatic gas exchange during hypoxia in armoured catfish

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Abstract

Air breathing in fish is commonly believed to have arisen as an adaptation to aquatic hypoxia. The effectiveness of air breathing for tissue O2 supply depends on the ability to avoid O2 loss as oxygenated blood from the air-breathing organ passes through the gills. Here, we evaluated whether the armoured catfish (Hypostomus aff. pyreneusi)—a facultative air breather—can avoid branchial O2 loss while air breathing in aquatic hypoxia, and we measured various other respiratory and metabolic traits important for O2 supply and utilization. Fish were instrumented with opercular catheters to measure the O2 tension (PO2) of expired water, and air breathing and aquatic respiration were measured during progressive stepwise hypoxia in the water. Armoured catfish exhibited relatively low rates of O2 consumption and gill ventilation, and gill ventilation increased in hypoxia due primarily to increases in ventilatory stroke volume. Armoured catfish began air breathing at a water PO2 of 2.5 kPa, and both air-breathing frequency and hypoxia tolerance (as reflected by PO2 at loss of equilibrium, LOE) was greater in individuals with a larger body mass. Branchial O2 loss, as reflected by higher PO2 in expired than in inspired water, was observed in a minority (4/11) of individuals as water PO2 approached that at LOE. Armoured catfish also exhibited a gill morphology characterized by short filaments bearing short fused lamellae, large interlamellar cell masses, low surface area, and a thick epithelium that increased water-to-blood diffusion distance. Armoured catfish had a relatively low blood-O2 binding affinity when sampled in normoxia (P50 of 3.1 kPa at pH 7.4), but were able to rapidly increase binding affinity during progressive hypoxia exposure (to a P50 of 1.8 kPa). Armoured catfish also had low activities of several metabolic enzymes in white muscle, liver, and brain. Therefore, low rates of metabolism and gill ventilation, and a reduction in branchial gas-exchange capacity, may help minimize branchial O2 loss in armoured catfish while air breathing in aquatic hypoxia.

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Acknowledgments

The authors would like to thank Grant McClelland, Chris Wood, Colin Brauner, Jeff Richards, Kevin Brix, and all other researchers on the Ana Clara expedition for many useful and entertaining discussions. We are also grateful to Jansen Alfredo Sampaio Zuanon for assistance with taxonomic identification, to Maria de Nazaré Paula da Silva and Raimunda Brandão for logistic support, and to the support staff aboard the Ana Clara for their hard work and for several excellent meals. Finally, we thank three anonymous referees for their helpful comments on an earlier version of this manuscript. This research was supported by FAPEAM and CNPq (Brazil) through the INCT-ADAPTA Grant to ALV and VMFAV, Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to GRS, KMG, and SFP, as well as funds to GRS from McMaster University, the Canadian Foundation for Innovation, and the Ontario Ministry of Research and Innovation. GRS is supported by the Canada Research Chairs Program, and ALV and VMFAV are recipients of research fellowships from CNPq.

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Authors and Affiliations

  1. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

    Graham R. Scott & Julie-Anne Mendoza

  2. Department of Biology, Center for Inland Waters, San Diego State University, San Diego, CA, 92182-4614, USA

    Victoria Matey

  3. Department of Biology, University of Ottawa, 30 Marie Curie Drive, Ottawa, ON, K1N 6N5, Canada

    Kathleen M. Gilmour & Steve F. Perry

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

    Vera M. F. Almeida-Val & Adalberto L. Val

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  1. Graham R. Scott
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  2. Victoria Matey
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  3. Julie-Anne Mendoza
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  4. Kathleen M. Gilmour
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  5. Steve F. Perry
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  6. Vera M. F. Almeida-Val
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  7. Adalberto L. Val
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Correspondence to Graham R. Scott.

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Communicated by G. Heldmaier.

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Scott, G.R., Matey, V., Mendoza, JA. et al. Air breathing and aquatic gas exchange during hypoxia in armoured catfish. J Comp Physiol B 187, 117–133 (2017). https://doi.org/10.1007/s00360-016-1024-y

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  • DOI: https://doi.org/10.1007/s00360-016-1024-y

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