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Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner

Aerobic metabolism generates 15–20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. For ectothermic water‐breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hen...

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Autores principales: Verberk, Wilco C. E. P., Sandker, Jeroen F., van de Pol, Iris L. E., Urbina, Mauricio A., Wilson, Rod W., McKenzie, David J., Leiva, Félix P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9542040/
https://www.ncbi.nlm.nih.gov/pubmed/35876025
http://dx.doi.org/10.1111/gcb.16319
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author Verberk, Wilco C. E. P.
Sandker, Jeroen F.
van de Pol, Iris L. E.
Urbina, Mauricio A.
Wilson, Rod W.
McKenzie, David J.
Leiva, Félix P.
author_facet Verberk, Wilco C. E. P.
Sandker, Jeroen F.
van de Pol, Iris L. E.
Urbina, Mauricio A.
Wilson, Rod W.
McKenzie, David J.
Leiva, Félix P.
author_sort Verberk, Wilco C. E. P.
collection PubMed
description Aerobic metabolism generates 15–20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. For ectothermic water‐breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hence aerobic metabolism. Here, we assess, within a phylogenetic context, how abiotic and biotic drivers explain the variation in hypoxia tolerance observed in fishes. To do so, we assembled a database of hypoxia tolerance, measured as critical oxygen tensions (P (crit)) for 195 fish species. Overall, we found that hypoxia tolerance has a clear phylogenetic signal and is further modulated by temperature, body mass, cell size, salinity and metabolic rate. Marine fishes were more susceptible to hypoxia than freshwater fishes. This pattern is consistent with greater fluctuations in oxygen and temperature in freshwater habitats. Fishes with higher oxygen requirements (e.g. a high metabolic rate relative to body mass) also were more susceptible to hypoxia. We also found evidence that hypoxia and warming can act synergistically, as hypoxia tolerance was generally lower in warmer waters. However, we found significant interactions between temperature and the body and cell size of a fish. Constraints in oxygen uptake related to cellular surface area to volume ratios and effects of viscosity on the thickness of the boundary layers enveloping the gills could explain these thermal dependencies. The lower hypoxia tolerance in warmer waters was particularly pronounced for fishes with larger bodies and larger cell sizes. Previous studies have found a wide diversity in the direction and strength of relationships between P (crit) and body mass. By including interactions with temperature, our study may help resolve these divergent findings, explaining the size dependency of hypoxia tolerance in fish.
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spelling pubmed-95420402022-10-14 Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner Verberk, Wilco C. E. P. Sandker, Jeroen F. van de Pol, Iris L. E. Urbina, Mauricio A. Wilson, Rod W. McKenzie, David J. Leiva, Félix P. Glob Chang Biol Research Articles Aerobic metabolism generates 15–20 times more energy (ATP) than anaerobic metabolism, which is crucial in maintaining energy budgets in animals, fueling metabolism, activity, growth and reproduction. For ectothermic water‐breathers such as fishes, low dissolved oxygen may limit oxygen uptake and hence aerobic metabolism. Here, we assess, within a phylogenetic context, how abiotic and biotic drivers explain the variation in hypoxia tolerance observed in fishes. To do so, we assembled a database of hypoxia tolerance, measured as critical oxygen tensions (P (crit)) for 195 fish species. Overall, we found that hypoxia tolerance has a clear phylogenetic signal and is further modulated by temperature, body mass, cell size, salinity and metabolic rate. Marine fishes were more susceptible to hypoxia than freshwater fishes. This pattern is consistent with greater fluctuations in oxygen and temperature in freshwater habitats. Fishes with higher oxygen requirements (e.g. a high metabolic rate relative to body mass) also were more susceptible to hypoxia. We also found evidence that hypoxia and warming can act synergistically, as hypoxia tolerance was generally lower in warmer waters. However, we found significant interactions between temperature and the body and cell size of a fish. Constraints in oxygen uptake related to cellular surface area to volume ratios and effects of viscosity on the thickness of the boundary layers enveloping the gills could explain these thermal dependencies. The lower hypoxia tolerance in warmer waters was particularly pronounced for fishes with larger bodies and larger cell sizes. Previous studies have found a wide diversity in the direction and strength of relationships between P (crit) and body mass. By including interactions with temperature, our study may help resolve these divergent findings, explaining the size dependency of hypoxia tolerance in fish. John Wiley and Sons Inc. 2022-07-25 2022-10 /pmc/articles/PMC9542040/ /pubmed/35876025 http://dx.doi.org/10.1111/gcb.16319 Text en © 2022 The Authors. Global Change Biology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Verberk, Wilco C. E. P.
Sandker, Jeroen F.
van de Pol, Iris L. E.
Urbina, Mauricio A.
Wilson, Rod W.
McKenzie, David J.
Leiva, Félix P.
Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title_full Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title_fullStr Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title_full_unstemmed Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title_short Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
title_sort body mass and cell size shape the tolerance of fishes to low oxygen in a temperature‐dependent manner
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9542040/
https://www.ncbi.nlm.nih.gov/pubmed/35876025
http://dx.doi.org/10.1111/gcb.16319
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