{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T21:09:23Z","timestamp":1791666563540,"version":"4.3.4"},"reference-count":83,"publisher":"Wiley","issue":"19","license":[{"start":{"date-parts":[[2022,7,25]],"date-time":"2022-07-25T00:00:00Z","timestamp":1658707200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002850","name":"Fondo Nacional de Desarrollo Cient\u00edfico y Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["1210071"],"award-info":[{"award-number":["1210071"]}],"id":[{"id":"10.13039\/501100002850","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002850","name":"Fondo Nacional de Desarrollo Cient\u00edfico y Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["2018\u201072190288"],"award-info":[{"award-number":["2018\u201072190288"]}],"id":[{"id":"10.13039\/501100002850","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003246","name":"Nederlandse Organisatie voor Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["016.161.321"],"award-info":[{"award-number":["016.161.321"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Global Change Biology"],"published-print":{"date-parts":[[2022,10]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Aerobic metabolism generates 15\u201320 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\u2010breathers 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 (\n                    <jats:italic>P<\/jats:italic>\n                    <jats:sub>crit<\/jats:sub>\n                    ) 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\n                    <jats:italic>P<\/jats:italic>\n                    <jats:sub>crit<\/jats:sub>\n                    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.\n                  <\/jats:p>","DOI":"10.1111\/gcb.16319","type":"journal-article","created":{"date-parts":[[2022,7,25]],"date-time":"2022-07-25T05:01:06Z","timestamp":1658725266000},"page":"5695-5707","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":83,"title":["Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature\u2010dependent manner"],"prefix":"10.1111","volume":"28","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0691-583X","authenticated-orcid":false,"given":"Wilco C. E. P.","family":"Verberk","sequence":"first","affiliation":[{"name":"Department of Animal Ecology and Physiology Radboud Institute for Biological and Environmental Sciences Radboud University Nijmegen Nijmegen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeroen F.","family":"Sandker","sequence":"additional","affiliation":[{"name":"Department of Animal Ecology and Physiology Radboud Institute for Biological and Environmental Sciences Radboud University Nijmegen Nijmegen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2962-6686","authenticated-orcid":false,"given":"Iris L. E.","family":"van de Pol","sequence":"additional","affiliation":[{"name":"Department of Animal Ecology and Physiology Radboud Institute for Biological and Environmental Sciences Radboud University Nijmegen Nijmegen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8040-6147","authenticated-orcid":false,"given":"Mauricio A.","family":"Urbina","sequence":"additional","affiliation":[{"name":"Departamento de Zoolog\u00eda, Facultad de Ciencias Naturales y Oceanogr\u00e1ficas Universidad de Concepci\u00f3n Concepci\u00f3n Chile"},{"name":"Instituto Milenio de Oceanograf\u00eda (IMO) Universidad de Concepci\u00f3n Concepci\u00f3n Chile"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8832-0065","authenticated-orcid":false,"given":"Rod W.","family":"Wilson","sequence":"additional","affiliation":[{"name":"Biosciences, University of Exeter Exeter UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0961-9101","authenticated-orcid":false,"given":"David J.","family":"McKenzie","sequence":"additional","affiliation":[{"name":"MARBEC, University of Montpellier, CNRS, IFREMER, IRD Montpellier France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0249-9274","authenticated-orcid":false,"given":"F\u00e9lix P.","family":"Leiva","sequence":"additional","affiliation":[{"name":"Department of Animal Ecology and Physiology Radboud Institute for Biological and Environmental Sciences Radboud University Nijmegen Nijmegen The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2022,7,25]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpa.2007.11.004"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1525\u2010142X.2006.00090.x"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-020-1171-0"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010021\u201021655\u2010w"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aao6868"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.066183"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abe5163"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aam7240"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v080.i01"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.32614\/RJ-2018-017"},{"key":"e_1_2_8_12_1","unstructured":"B\u00fcrkner P.\u2010C.(2021).Estimating phylogenetic multilevel models with brms.https:\/\/cran.r\u2010project.org\/web\/packages\/brms\/vignettes\/brms_phylogenetics.html"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365\u20102486.2009.01995.x"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1111\/jfb.12833"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365\u20102656.1999.00337.x"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.232512"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.aaz3658"},{"key":"e_1_2_8_18_1","volume-title":"Principles of comparative respiratory physiology","author":"Dejours P.","year":"1981"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586\u2010020\u20102721\u2010y"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10577-011-9248-x"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1111\/jfb.12330"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1080\/00031305.2018.1549100"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.1989.0106"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1006\/bcmd.2001.0457"},{"key":"e_1_2_8_25_1","unstructured":"Gregory T. R.(2021).Animal genome size database.www.genomesize.com"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1007\/BFb0030909"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1420\u20109101.2009.01915.x"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btm538"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev\u2010ento\u2010020117\u2010043145"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.243421"},{"key":"e_1_2_8_31_1","unstructured":"Henry L. &Wickham H.(2020).Purrr: Functional programming tools. R package version 0.3.4.https:\/\/cran.r-project.org\/package=purrr"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.227124"},{"key":"e_1_2_8_33_1","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780195117028.001.0001","volume-title":"Biochemical adaptation. Mechanism and process in physiological evolution","author":"Hochachka P. W.","year":"2002"},{"key":"e_1_2_8_34_1","doi-asserted-by":"publisher","DOI":"10.1111\/ele.12413"},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586\u2010021\u201003550\u2010y"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2435.13811"},{"key":"e_1_2_8_37_1","unstructured":"Kay M.(2021).tidybayes: Tidy data and geoms for Bayesian models. R package version 3.0.1.http:\/\/mjskay.github.io\/tidybayes\/"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2435.13449"},{"key":"e_1_2_8_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1461-0248.2009.01415.x"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1086\/685893"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12615"},{"key":"e_1_2_8_42_1","doi-asserted-by":"publisher","DOI":"10.1111\/gcb.13652"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2019.0035"},{"key":"e_1_2_8_44_1","doi-asserted-by":"publisher","DOI":"10.1111\/gcb.16067"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jtherbio.2019.07.029"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365\u20102435.2011.01870.x"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.21105\/joss.01541"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1002\/evl3.243"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2008.1235"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2100695118"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.1111\/2041-210X.12593"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.1002\/bies.201700058"},{"key":"e_1_2_8_53_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469\u2010185X.2008.00038.x"},{"key":"e_1_2_8_54_1","unstructured":"Orme D. Freckleton R. Thomas G. Petzoldt T. Fritz S. Isaac N. &Pearse W.(2018).caper: Comparative analyses of phylogenetics and evolution in R. R package version 1.0.1.https:\/\/cran.r-project.org\/package=caper"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/bty633"},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abc6050"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btu181"},{"key":"e_1_2_8_58_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0229468"},{"key":"e_1_2_8_59_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-185X.1955.tb01208.x"},{"key":"e_1_2_8_60_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.100.1.275"},{"key":"e_1_2_8_61_1","doi-asserted-by":"publisher","DOI":"10.1016\/0300-9629(72)90017-5"},{"key":"e_1_2_8_62_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.2041-210X.2011.00169.x"},{"key":"e_1_2_8_63_1","doi-asserted-by":"publisher","DOI":"10.1002\/cphy.c100079"},{"key":"e_1_2_8_64_1","unstructured":"Rogers N. J. Urbina M. A. Reardon E. E. McKenzie D. J. Birchenough S. N. R. &Wilson R. W.(2021).Database of critical oxygen level(Pcrit)in freshwater and marine fishes 1974\u20142015\u2014Cefas(Centre for Environment Fisheries and Aquaculture Science). https:\/\/www.cefas.co.uk\/data\u2010and\u2010publications\/dois\/database\u2010of\u2010critical\u2010oxygen\u2010level\u2010pcrit\u2010in\u2010freshwater\u2010and\u2010marine\u2010fishes\u20101974\u20102015\/"},{"key":"e_1_2_8_65_1","doi-asserted-by":"publisher","DOI":"10.1093\/conphys\/cow012"},{"key":"e_1_2_8_66_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2003292117"},{"key":"e_1_2_8_67_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.210492"},{"key":"e_1_2_8_68_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1153847"},{"key":"e_1_2_8_69_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.86.12.4474"},{"key":"e_1_2_8_70_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0022\u20105193(83)80002\u20102"},{"key":"e_1_2_8_71_1","doi-asserted-by":"publisher","DOI":"10.1086\/673727"},{"key":"e_1_2_8_72_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11222-016-9696-4"},{"key":"e_1_2_8_73_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365\u20102435.12152"},{"key":"e_1_2_8_74_1","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12653"},{"key":"e_1_2_8_75_1","doi-asserted-by":"publisher","DOI":"10.1890\/10\u20102369.1"},{"key":"e_1_2_8_76_1","doi-asserted-by":"publisher","DOI":"10.1111\/gcb.13240"},{"key":"e_1_2_8_77_1","doi-asserted-by":"crossref","unstructured":"Verberk W. C. E. P. Sandkler J. F. van delPol I. L. E. UrbinaM. A. WilsonR. W. McKenzie D. J. &Leiva F. P.(2022).Data and code for: Body mass and cell size shape the tolerance of fishes to low oxygen in a temperature\u2010dependent manner.Zenodo.https:\/\/doi.org\/10.5281\/zenodo.6123770.","DOI":"10.1111\/gcb.16319"},{"key":"e_1_2_8_78_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msz240"},{"key":"e_1_2_8_79_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.88.22.10357"},{"key":"e_1_2_8_80_1","doi-asserted-by":"crossref","unstructured":"Wickham H.(2016).ggplot2: Elegant graphics for data analysis.https:\/\/ggplot2.tidyverse.org","DOI":"10.1007\/978-3-319-24277-4"},{"key":"e_1_2_8_81_1","unstructured":"Wickham H.(2019).Stringr: Simple consistent wrappers for common string operations. R package version 1.4.0.https:\/\/cran.r-project.org\/package=stringr"},{"key":"e_1_2_8_82_1","doi-asserted-by":"crossref","unstructured":"Wickham H. Francois R. Henry L. &M\u00fcller K.(2021).Dplyr: A grammar of data manipulation. R package version 1.0.7.https:\/\/cran.r-project.org\/package=dplyr","DOI":"10.1007\/978-1-4842-6876-6_1"},{"key":"e_1_2_8_83_1","doi-asserted-by":"publisher","DOI":"10.1093\/icb\/39.2.244"},{"key":"e_1_2_8_84_1","doi-asserted-by":"publisher","DOI":"10.1111\/2041-210X.12628"}],"container-title":["Global Change Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/gcb.16319","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/gcb.16319","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/gcb.16319","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,24]],"date-time":"2023-11-24T17:54:34Z","timestamp":1700848474000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/gcb.16319"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,25]]},"references-count":83,"journal-issue":{"issue":"19","published-print":{"date-parts":[[2022,10]]}},"alternative-id":["10.1111\/gcb.16319"],"URL":"https:\/\/doi.org\/10.1111\/gcb.16319","archive":["Portico"],"relation":{},"ISSN":["1354-1013","1365-2486"],"issn-type":[{"value":"1354-1013","type":"print"},{"value":"1365-2486","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,25]]},"assertion":[{"value":"2021-12-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-05-22","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-07-25","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}