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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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2022
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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. |
format | Online Article Text |
id | pubmed-9542040 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
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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