{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,7]],"date-time":"2026-07-07T05:14:53Z","timestamp":1783401293679,"version":"3.54.6"},"reference-count":99,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T00:00:00Z","timestamp":1783036800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Portuguese Foundation for Science and Technology","award":["UIDB\/04292\/2020"],"award-info":[{"award-number":["UIDB\/04292\/2020"]}]},{"name":"Portuguese Foundation for Science and Technology","award":["LA\/P\/0069\/2020"],"award-info":[{"award-number":["LA\/P\/0069\/2020"]}]},{"name":"FSE","award":["SFRH\/BPD\/117533\/2016"],"award-info":[{"award-number":["SFRH\/BPD\/117533\/2016"]}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["2023.08477.CEECIND\/CP2831\/CT0014"],"award-info":[{"award-number":["2023.08477.CEECIND\/CP2831\/CT0014"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["2020.00174.CEECIND\/CP1605\/CT0003"],"award-info":[{"award-number":["2020.00174.CEECIND\/CP1605\/CT0003"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["10.54499\/2020.00174.CEECIND\/CP1605\/CT0003"],"award-info":[{"award-number":["10.54499\/2020.00174.CEECIND\/CP1605\/CT0003"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["SFRH\/BD\/117890\/ 2016"],"award-info":[{"award-number":["SFRH\/BD\/117890\/ 2016"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["SFRH\/BD\/111691\/2015"],"award-info":[{"award-number":["SFRH\/BD\/111691\/2015"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT Scientific Employment Stimulus program","doi-asserted-by":"publisher","award":["SFRH\/BD\/131771\/2017"],"award-info":[{"award-number":["SFRH\/BD\/131771\/2017"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"name":"TRANSFISH","award":["PTCD\/BIA-BMA\/28647\/2017"],"award-info":[{"award-number":["PTCD\/BIA-BMA\/28647\/2017"]}]},{"name":"TRANSFISH","award":["LISBOA-01-0145-FEDER-028647"],"award-info":[{"award-number":["LISBOA-01-0145-FEDER-028647"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>The interaction between increased dissolved carbon dioxide, rising temperatures, and oxygen loss\u2014the so-called \u201cdeadly trio\u201d\u2014is expected to strongly affect marine biota over the coming years, undermining ocean services and uses. Nonetheless, no study has so far scrutinized the cumulative impact of these three stressors on fish embryos and larvae. To fill this knowledge gap, we conducted a fully multi-factorial experiment to investigate the effects of warming (+4 \u00b0C: 22 \u00b0C), acidification (\u0394 \u2212 0.4 pH units: 7.7 pH, pCO2 ~1000 \u03bcatm), and deoxygenation (\u0394 \u2212 60% O2 saturation: 3 mg O2 L\u22121) on physiological and behavioral responses of the commercially important species Sparus aurata. Deoxygenation was the primary factor reducing hatching rates (64.25%), survival (46.71%), and heart rates (31.99%) of recently hatched larvae, being generally further exacerbated when combined with warming and acidification. No larvae exposed to the interaction of the three treatments reacted to the phototactic behavior test. However, acidification alone caused a 50% reduction in phototactic behavior. Our findings demonstrate that the deadly trio is detrimental to early fish development, impacting several key features at this critical life stage, and the need to assess the impacts of stressors\u2019 interaction on marine taxa to better predict future ecosystem responses to ocean changes.<\/jats:p>","DOI":"10.3390\/biology15131068","type":"journal-article","created":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T14:33:06Z","timestamp":1783089186000},"page":"1068","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Impacts of Warming, Acidification, and Deoxygenation on Embryos and Larvae of Gilthead Seabream (Sparus aurata)"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3248-4479","authenticated-orcid":false,"given":"Marta S.","family":"Pimentel","sequence":"first","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"},{"name":"Department of Animal Biology, Faculty of Science, University of Lisbon, 1749-016 Lisbon, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Catarina P.","family":"Santos","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria R.","family":"Pegado","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eduardo","family":"Sampaio","sequence":"additional","affiliation":[{"name":"Department of Collective Behaviour, Centre for the Advanced Study of Collective Behaviour, University of Konstanz, 78464 Konstanz, Germany"},{"name":"Department of Animal Biology, University of Konstanz, 78464 Konstanz, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6746-764X","authenticated-orcid":false,"given":"Pedro","family":"Pous\u00e3o-Ferreira","sequence":"additional","affiliation":[{"name":"Instituto Portugu\u00eas do Mar e da Atmosfera, Av. 5 de Outubro s\/n, 8700-305 Olh\u00e3o, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanessa M.","family":"Lopes","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-4227-8782","authenticated-orcid":false,"given":"David Abreu dos","family":"Santos","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-6545-7444","authenticated-orcid":false,"given":"Jo\u00e3o","family":"Caramelo","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2801-5178","authenticated-orcid":false,"given":"Rui","family":"Rosa","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre\/ARNET\u2013Aquatic Research Network, Laborat\u00f3rio Mar\u00edtimo da Guia, Faculdade de Ci\u00eancias, Universidade de Lisboa, Av. Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal"},{"name":"Department of Animal Biology, Faculty of Science, University of Lisbon, 1749-016 Lisbon, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,3]]},"reference":[{"key":"ref_1","unstructured":"Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, V., Nauels, A., Xia, Y., Bex, V., and Midgley, P.M. (2013). Climate Change 2013: The Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"20160325","DOI":"10.1098\/rsta.2016.0325","article-title":"Patterns of deoxygenation: Sensitivity to natural and anthropogenic drivers","volume":"375","author":"Oschlies","year":"2017","journal-title":"Philos. Trans. R. Soc. A Math. Phys. Eng. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"eaam7240","DOI":"10.1126\/science.aam7240","article-title":"Declining oxygen in the global ocean and coastal waters","volume":"359","author":"Breitburg","year":"2018","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1146\/annurev-marine-121916-063359","article-title":"Manifestation, drivers, and emergence of open ocean deoxygenation","volume":"10","author":"Levin","year":"2018","journal-title":"Annu. Rev. Mar. Sc."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Laffoley, D., and Baxter, J.M. (2019). Ocean Deoxygenation: Everyone\u2019s Problem\u2014Causes, Impacts, Consequences and Solutions, IUCN.","DOI":"10.2305\/IUCN.CH.2019.13.en"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1111\/gcb.14879","article-title":"Defining CO2 and O2 syndromes of marine biomes in the Anthropocene","volume":"26","author":"Klein","year":"2020","journal-title":"Glob. Change Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1002\/2015GB005338","article-title":"Sources of uncertainties in 21st century projections of potential ocean ecosystem stressors","volume":"30","author":"Rodgers","year":"2016","journal-title":"Glob. Biogeochem. Cycles"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"20150976","DOI":"10.1098\/rsbl.2015.0976","article-title":"Hypoxia and acidification in ocean ecosystems: Coupled dynamics and effects on marine life","volume":"12","author":"Gobler","year":"2016","journal-title":"Biol. Lett."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"162","DOI":"10.5670\/oceanog.2018.205","article-title":"Categorizing and naming marine heatwaves","volume":"31","author":"Hobday","year":"2018","journal-title":"Oceanography"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1038\/s41467-018-03732-9","article-title":"Longer and more frequent marine heatwaves over the past century","volume":"9","author":"Oliver","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"4633","DOI":"10.5194\/bg-17-4633-2020","article-title":"Increase in ocean acidity variability and extremes under increasing atmospheric CO2","volume":"17","author":"Burger","year":"2020","journal-title":"Biogeosciences"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Schulz, K.G., Hartley, S., and Eyre, B. (2019). Upwelling amplifies ocean acidification on the East Australian Shelf: Implications for marine ecosystems. Front. Mar. Sci., 6.","DOI":"10.3389\/fmars.2019.00636"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/s41559-020-01370-3","article-title":"Impacts of hypoxic events surpass those of future ocean warming and acidification","volume":"5","author":"Sampaio","year":"2021","journal-title":"Nat. Ecol. Evol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S1546-5098(08)60199-5","article-title":"Respiratory Gas Exchange, Aerobic Metabolism, and Effects of Hypoxia During Early Life","volume":"11","author":"Rombough","year":"1988","journal-title":"Fish Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"20161868","DOI":"10.1098\/rspb.2016.1868","article-title":"Acute embryonic anoxia exposure favours the development of a dominant and aggressive phenotype in adult zebrafish","volume":"284","author":"Ivy","year":"2016","journal-title":"Proc. R. Soc. B"},{"key":"ref_16","first-page":"1846","article-title":"An early life hypoxia event has a long-term impact on protein digestion and growth in juvenile European sea bass","volume":"220","author":"Mazurais","year":"2017","journal-title":"J. Exp. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1002\/ece3.516","article-title":"Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming","volume":"3","author":"Harvey","year":"2013","journal-title":"Ecol. Evol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"20180408","DOI":"10.1098\/rsbl.2018.0408","article-title":"Robust quantification of fish early life CO2 sensitivities via serial experimentation","volume":"14","author":"Baumann","year":"2018","journal-title":"Biol. Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/s00227-024-04439-w","article-title":"The combined effects of ocean warming and ocean acidification on Pacific cod early life stages","volume":"171","author":"Slesinger","year":"2024","journal-title":"Mar. Biol."},{"key":"ref_20","first-page":"2748","article-title":"Hidden impacts of ocean warming and acidification on biological responses of marine animals revealed through meta-analysis","volume":"15","author":"Alter","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1038\/nclimate1291","article-title":"Reduced early life growth and survival in a fish in direct response to increased carbon dioxide","volume":"2","author":"Baumann","year":"2012","journal-title":"Nat. Clim. Change"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3865","DOI":"10.1242\/jeb.074765","article-title":"Impact of global warming and rising CO2 levels on coral reef fishes: What hope for the future?","volume":"215","author":"Munday","year":"2012","journal-title":"J. Exp. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1890\/13-0297.1","article-title":"Organ damage in Atlantic herring larvae as a result of ocean acidification","volume":"24","author":"Frommel","year":"2014","journal-title":"Ecol. Appl."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"145","DOI":"10.3354\/meps11142","article-title":"Vulnerability of early life stage Northwest Atlantic forage fish to ocean acidification and low oxygen","volume":"523","author":"DePasquale","year":"2015","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_25","first-page":"2062","article-title":"Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean","volume":"217","author":"Pimentel","year":"2014","journal-title":"J. Exp. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"0134082","DOI":"10.1371\/journal.pone.0134082","article-title":"Oxidative stress and digestive enzyme activity of flatfish larvae in a changing ocean","volume":"10","author":"Pimentel","year":"2015","journal-title":"PLoS ONE"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1007\/s10584-016-1682-5","article-title":"Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming","volume":"137","author":"Pimentel","year":"2016","journal-title":"Clim. Change"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/fishes5010001","article-title":"Seabream larval physiology under ocean warming and acidification","volume":"5","author":"Pimentel","year":"2020","journal-title":"Fishes"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Laubenstein, T.D., Rummer, J.L., Nicol, S., Parsons, D.M., Pether, S.M.J., Pope, S., and Munday, P.L. (2018). Correlated effects of ocean acidification and warming on behavioral and metabolic traits of a large pelagic fish. Diversity, 10.","DOI":"10.3390\/d10020035"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"4368","DOI":"10.1111\/gcb.14290","article-title":"Ocean warming has a greater effect than acidification on the early life history development and swimming performance of a large circumglobal pelagic fish","volume":"24","author":"Watson","year":"2018","journal-title":"Glob. Change Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e0221283","DOI":"10.1371\/journal.pone.0221283","article-title":"Combined effects of ocean acidification and temperature on larval and juvenile growth, development and swimming performance of European sea bass (Dicentrarchus labrax)","volume":"14","author":"Cominassi","year":"2019","journal-title":"PLoS ONE"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"jeb212589","DOI":"10.1242\/jeb.212589","article-title":"Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation","volume":"223","author":"Dahlke","year":"2020","journal-title":"J. Exp. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.marenvres.2018.03.011","article-title":"Moderate hypoxia but not warming conditions at larval stages induces adverse carry-over effects on hypoxia tolerance of European sea bass (Dicentrarchus labrax) juveniles","volume":"138","author":"Cadiz","year":"2018","journal-title":"Mar. Environ. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1093\/icb\/ict066","article-title":"Responses to temperature and hypoxia as interacting stressors in fish: Implications for adaptation to environmental change","volume":"53","author":"McBryan","year":"2013","journal-title":"Integr. Comp. Biol."},{"key":"ref_35","first-page":"coy078","article-title":"Combined effects of warming and hypoxia on early life stage Chinook salmon physiology and development","volume":"7","author":"Rio","year":"2019","journal-title":"Conserv. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Leal Filho, W., Azul, A.M., Brandli, L., \u00d6zuyar, P.G., and Wall, T. (2020). Climate change, multiple stressors and responses of marine biota. Encyclopedia of the UN Sustainable Development Goals. Climate Action, Springer Nature.","DOI":"10.1007\/978-3-319-71063-1"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1086\/721468","article-title":"Impacts of low oxygen on marine life: Neglected but a crucial priority for research","volume":"243","author":"Borges","year":"2022","journal-title":"Biol. Bull."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1980","DOI":"10.1098\/rsta.2011.0003","article-title":"Warming up, turning sour, losing breath: Ocean biogeochemistry under global change","volume":"369","author":"Gruber","year":"2011","journal-title":"Philos. Trans. R. Soc. A"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1146\/annurev-marine-041911-111611","article-title":"Climate change impacts on marine ecosystems","volume":"4","author":"Doney","year":"2012","journal-title":"Annu. Rev. Mar. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"273","DOI":"10.3354\/meps10123","article-title":"Integrating climate-related stressor effects on marine organisms: Unifying principles linking molecule to ecosystem-level changes","volume":"470","year":"2012","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_41","first-page":"1","article-title":"Combined effects of ocean acidification, warming, and hypoxia on marine organisms","volume":"6","author":"Baumann","year":"2016","journal-title":"Limnol. Oceanogr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1139\/cjz-2018-0198","article-title":"Experimental assessments of marine species sensitivities to ocean acidification and co-stressors: How far have we come?","volume":"97","author":"Baumann","year":"2019","journal-title":"Can. J. Zool."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jembe.2017.09.002","article-title":"Metabolic response and thermal tolerance of green abalone juveniles (Haliotis fulgens: Gastropoda) under acute hypoxia and hypercapnia","volume":"497","author":"Bock","year":"2017","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref_44","first-page":"110438","article-title":"Single and combined effects of the \u201cDeadly trio\u201d hypoxia, hypercapnia and warming on the cellular metabolism of the great scallop Pecten maximus","volume":"243\u2013244","author":"Bock","year":"2020","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1111\/j.1461-0248.2008.01253.x","article-title":"Interactive and cumulative effects of multiple human stressors in marine systems","volume":"11","author":"Crain","year":"2008","journal-title":"Ecol. Lett."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1093\/icb\/ict086","article-title":"Physiological responses to shifts in multiple environmental stressors: Relevance in a changing world","volume":"53","author":"Todgham","year":"2013","journal-title":"Integr. Comp. Biol."},{"key":"ref_47","unstructured":"Barange, M., Bahri, T., Beveridge, M.C.M., Cochrane, K.L., Funge-Smith, S., and Poulain, F. (2018). Impacts of Climate Change on Fisheries and Aquaculture: Synthesis of Current Knowledge, Adaptation and Mitigation Options, Food and Agriculture Organization of the United Nations. FAO Fisheries and Aquaculture Technical Paper 627."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1038\/s41893-020-0513-x","article-title":"Integrating climate change in ocean planning","volume":"3","author":"Agardy","year":"2020","journal-title":"Nat. Sustain."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1016\/j.ecss.2008.06.019","article-title":"Site fidelity and movements of gilthead sea bream (Sparus aurata) in a coastal lagoon (Ria Formosa, Portugal)","volume":"79","author":"Abecasis","year":"2008","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3354\/meps09444","article-title":"Multi-element otolith fingerprints unravel sea\u2212lagoon lifetime migrations of gilthead sea bream Sparus aurata","volume":"444","author":"Mercier","year":"2012","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/S0044-8486(01)00527-0","article-title":"Long photoperiod delayed spawning and increased somatic growth in gilthead seabream (Sparus aurata)","volume":"200","author":"Kissil","year":"2001","journal-title":"Aquaculture"},{"key":"ref_52","first-page":"48","article-title":"Negative synergistic impacts of ocean warming and acidification on the survival and proteome of the commercial sea bream Sparus aurata","volume":"140","author":"Madeira","year":"2018","journal-title":"J. Sea Res."},{"key":"ref_53","first-page":"59","article-title":"Crecimiento, regimen alimentario y reproducci\u00f3n de la dorada (Sparus aurata L.) y del robalo (Dicentrarchus labrax L.) en los esteros de Cadiz","volume":"44","author":"Arias","year":"1980","journal-title":"Investig. Pesq."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/S0043-1354(98)00168-7","article-title":"A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples","volume":"33","author":"Sarazin","year":"1999","journal-title":"Water Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0044-8486(00)00446-4","article-title":"Skeletal descriptors and quality assessment in larvae and post- larvae of wild-caught and hatchery-reared gilthead sea bream (Sparus aurata L. 1758)","volume":"192","author":"Boglione","year":"2001","journal-title":"Aquaculture"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3637","DOI":"10.1002\/ece3.709","article-title":"Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish","volume":"3","author":"Forsgren","year":"2013","journal-title":"Ecol. Evol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Zuur, A.F., Ieno, E.N., Walker, N., Saveliev, A.A., and Smith, G.M. (2009). Mixed Effects Models and Extensions in Ecology with R, Springer.","DOI":"10.1007\/978-0-387-87458-6"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1016\/j.jml.2012.11.001","article-title":"Random effects structure for confirmatory hypothesis testing: Keep it maximal","volume":"68","author":"Barr","year":"2013","journal-title":"J. Mem. Lang."},{"key":"ref_59","unstructured":"Lenth, R. (2019). Emmeans: Estimated Marginal Means, aka Least-Squares Means, ScienceOpen."},{"key":"ref_60","first-page":"430","article-title":"Effects of reduced oxygen level on the mortality and hatching rate of Chondrostoma nasus embryos","volume":"49","author":"Keckeis","year":"1996","journal-title":"J. Fish Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1126\/science.1163156","article-title":"Physiology and Climate Change","volume":"322","author":"Farrell","year":"2008","journal-title":"Science"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1242\/jeb.037523","article-title":"Oxygen- and capacity-limitation of thermal tolerance: A matrix for integrating climate-related stressor effects in marine ecosystems","volume":"213","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.cbpb.2013.06.006","article-title":"Elevated temperature and PCO2 shift metabolic pathways in differentially oxidative tissues of Notothenia rossii","volume":"166","author":"Strobel","year":"2013","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1912","DOI":"10.1139\/z76-221","article-title":"Developmental rates of embryos of Atlantic salmon, Salmo salar L., in response to various levels of temperature, dissolved oxygen, and water exchange","volume":"54","author":"Hamor","year":"1959","journal-title":"Can. J. Zool."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1139\/f06-036","article-title":"Energy expenditure during hatching in rainbow trout (Oncorhynchus mykiss) embryos","volume":"63","author":"Ninness","year":"2006","journal-title":"Can. J. Fish. Aquat. Sci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.5194\/bg-11-1613-2014","article-title":"Effects of elevated CO2 in the early life stages of summer flounder, Paralichthys dentatus, and potential consequences of ocean acidification","volume":"11","author":"Chambers","year":"2014","journal-title":"Biogeosciences"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3354\/meps10791","article-title":"Offspring sensitivity to ocean acidification changes seasonally in a coastal marine fish","volume":"504","author":"Murray","year":"2014","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s00227-016-2898-7","article-title":"Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2 and warming","volume":"163","author":"Rosa","year":"2016","journal-title":"Mar. Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/BF00004375","article-title":"Cardiac activity, ventilation rate and acid-base regulation in rainbow trout exposed to hypoxia and combined hypoxia and hypercapnia","volume":"12","author":"Borch","year":"1993","journal-title":"Fish Physiol. Biochem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"R104","DOI":"10.1152\/ajpregu.00418.2009","article-title":"Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia","volume":"298","author":"Sandblom","year":"2010","journal-title":"Am. J. Physiol.-Regul. Integr. Comp. Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1111\/jfb.12833","article-title":"Responses by fishes to environmental hypoxia: Integration through Fry\u2019s concept of aerobic metabolic scope","volume":"88","author":"Claireaux","year":"2016","journal-title":"J. Fish Biol."},{"key":"ref_72","first-page":"302","article-title":"The effects of hypoxic bradycardia and extracellular HCO3\u2212\/CO2 on hypoxic performance in the eel heart","volume":"219","author":"Joyce","year":"2016","journal-title":"J. Exp. Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0025-326X(02)00061-9","article-title":"Hypoxia: From molecular responses to ecosystem responses","volume":"45","author":"Wu","year":"2002","journal-title":"Mar. Pollut. Bull."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Hochachka, P.W., and Somero, G.N. (2002). Biochemical Adaptation: Mechanisms and Process in Physiological Evolution, Oxford University Press.","DOI":"10.1093\/oso\/9780195117028.001.0001"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1007\/s10872-004-5763-0","article-title":"Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history","volume":"60","author":"Langenbuch","year":"2004","journal-title":"J. Oceanogr."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Storey, K.B. (2004). Oxygen limitation and metabolic rate depression. Functional Metabolism: Regulation and Adaptation, Wiley.","DOI":"10.1002\/047167558X.ch15"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"203","DOI":"10.3354\/meps07768","article-title":"Ecosystem effects of ocean acidification in times of ocean warming: A physiologist\u2019s view","volume":"373","year":"2008","journal-title":"Mar. Ecol. Prog."},{"key":"ref_78","first-page":"1","article-title":"Effects of hypoxia on buoyancy control and the development of lordosis in physostomous and physoclistous fish species","volume":"5","author":"Bagowski","year":"2011","journal-title":"Res. Rev. Biosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.4067\/S0717-95022011000400036","article-title":"Vertebral Column Deformity and Hypoxia in Salmo salar","volume":"29","author":"Rauco","year":"2011","journal-title":"Int. J. Morphol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1111\/jfd.12417","article-title":"Ocean acidification leads to deformations of caudal vein angio-architecture in juvenile threespine stickleback, Gasterosteus aculeatus Linnaeus","volume":"39","author":"Ahnelt","year":"2015","journal-title":"J. Fish Dis."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1086\/physzool.57.1.30155967","article-title":"Developmental and oxygen consumption rate differences between lactate dehydrogenase-B genotypes of Fundulus heteroclitus and their effect on hatching time","volume":"57","author":"DiMichele","year":"1984","journal-title":"Physiol. Zool."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1139\/f89-008","article-title":"Oxygen availability provided a signal for hatching in the rainbow trout (Salmo gairdneri) embryo","volume":"46","author":"Latham","year":"1989","journal-title":"Can. J. Fish. Aquat. Sci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/S0044-8486(00)00545-7","article-title":"Critical partial pressures of oxygen causing precocious hatching in Coregonus lavaretus and C. albula embryos","volume":"196","author":"Czerkies","year":"2001","journal-title":"Aquaculture"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"850\u2212858","DOI":"10.1111\/j.1365-2109.2004.01076.x","article-title":"Oxygen deficiency during somitogenesis causes centrum defects in red sea bream, Pagrus major (Temminck et Schlegel)","volume":"35","author":"Hattori","year":"2004","journal-title":"Aquac. Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"59","DOI":"10.3354\/dao02056","article-title":"Effects of skeletal deformities on swimming performance and recovery from exhaustive exercise in triploid Atlantic salmon","volume":"85","author":"Powell","year":"2009","journal-title":"Dis. Aquat. Org."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1093\/icesjms\/23.2.213","article-title":"Reactions of fish to artificial light, with special reference to large herring and spring herring in Norway","volume":"23","author":"Dragesund","year":"1958","journal-title":"ICES J. Mar. Sci."},{"key":"ref_87","unstructured":"Ben-Yami, M. (1976). Fishing with Light, Fishing News Books."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.fishres.2004.12.009","article-title":"Behavioural effects of artificial light on fish species of commercial interest","volume":"73","author":"Marchesan","year":"2005","journal-title":"Fish. Res."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Kamler, E. (1992). Mixed feeding period, and 6. Early exogenous feeding period. Early Life History of Fish\u2014An Energetics Approach, Chapman & Hall.","DOI":"10.1007\/978-94-011-2324-2"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1046\/j.1365-2109.2001.00628.x","article-title":"A correlation between phototactic response and first-feeding of Atlantic halibut (Hippoglossus hippoglossus L.) larvae","volume":"32","author":"Karlsen","year":"2001","journal-title":"Aquac. Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S0065-2881(08)60202-3","article-title":"Plankton production and year-class strength in fish populations: An update of the match\/ mismatch hypothesis","volume":"26","author":"Cushing","year":"1990","journal-title":"Adv. Mar. Biol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1093\/icb\/icx010","article-title":"Impacts of ocean acidification on sensory function in marine organisms","volume":"57","author":"Ashur","year":"2017","journal-title":"Integr. Comp. Biol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1303","DOI":"10.1139\/f71-197","article-title":"Effect of oxygen depletion and carbon dioxide build-up on the phototactic behaviour of the walleye (Stizostedion vitreum vitreum Mitchill)","volume":"28","author":"Scherer","year":"1971","journal-title":"J. Fish Res. Bd. Can."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/j.anbehav.2011.12.014","article-title":"Principles of animal communication","volume":"83","author":"Bradbury","year":"2012","journal-title":"Anim. Behav."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/0044-8486(87)90171-2","article-title":"Energy budgets for juvenile rainbow trout at various oxygen concentrations","volume":"62","author":"Pedersen","year":"1987","journal-title":"Aquaculture"},{"key":"ref_96","first-page":"C09S10","article-title":"Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change","volume":"110","author":"Langenbuch","year":"2005","journal-title":"J. Geophys. Res. Ocean."},{"key":"ref_97","first-page":"95\u221297","article-title":"Climate change affects marine fishes through the oxygen limitation of thermal tolerance","volume":"315","author":"Knust","year":"2007","journal-title":"Science"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S1546-5098(08)00008-3","article-title":"The effects of hypoxia on growth and digestion","volume":"Volume 27","author":"Richards","year":"2009","journal-title":"Fish Physiology"},{"key":"ref_99","unstructured":"Collins, M. (2020). Extremes, abrupt changes and managing risks. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate, Intergovernmental Panel on Climate Change."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/13\/1068\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,7]],"date-time":"2026-07-07T04:20:40Z","timestamp":1783398040000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/13\/1068"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,3]]},"references-count":99,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["biology15131068"],"URL":"https:\/\/doi.org\/10.3390\/biology15131068","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,3]]}}}