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Impacts of deoxygenation and hypoxia on shark embryos anti-predator behavior and oxidative stress

2023Journal article Open access
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dc.contributor.authorVarela, Jaquelino
dc.contributor.authorMartins Rebocho, Sandra
dc.contributor.authorCourt, Melanie
dc.contributor.authorSantos, Catarina Pereira
dc.contributor.authorPaula, José Ricardo
dc.contributor.authorFerreira, Inês João
dc.contributor.authorDiniz, Mário
dc.contributor.authorRepolho, Tiago
dc.contributor.authorRosa, Rui
dc.date.accessioned2023-05-30T14:04:18Z
dc.date.available2023-05-30T14:04:18Z
dc.date.issued2023
dc.description.abstractSimple Summary Despite their importance, sharks are among the most endangered ocean species. In addition to overexploitation and the destruction of their natural habitat, climate change is also known to pose a serious threat to them. Among the physico-chemical changes associated with climate change, oxygen loss has been the least studied in terms of its effect on shark physiology and behavior. In this study, we evaluated the impact of deoxygenation (93% air saturation) and hypoxia (26% air saturation) on the anti-predatory behavior and physiology of temperate shark embryos. We found that hypoxia caused a high mortality (44%), significantly increased embryo movement within capsules, and, consequently, reduced the freezing response behavior (a behavior that allows embryos to be unnoticed by predators). Regarding oxidative stress, most biomarkers analyzed were not impacted by the experimental treatments. Overall, our results suggest that the temperate shark's early life stages showed a certain degree of resilience to deoxygenation but not to hypoxia. Climate change is leading to the loss of oxygen content in the oceans and endangering the survival of many marine species. Due to sea surface temperature warming and changing circulation, the ocean has become more stratified and is consequently losing its oxygen content. Oviparous elasmobranchs are particularly vulnerable as they lay their eggs in coastal and shallow areas, where they experience significant oscillations in oxygen levels. Here, we investigated the effects of deoxygenation (93% air saturation) and hypoxia (26% air saturation) during a short-term period (six days) on the anti-predator avoidance behavior and physiology (oxidative stress) of small-spotted catshark (Scyliorhinus canicula) embryos. Their survival rate decreased to 88% and 56% under deoxygenation and hypoxia, respectively. The tail beat rates were significantly enhanced in the embryos under hypoxia compared to those exposed to deoxygenation and control conditions, and the freeze response duration showed a significant opposite trend. Yet, at the physiological level, through the analyses of key biomarkers (SOD, CAT, GPx, and GST activities as well as HSP70, Ubiquitin, and MDA levels), we found no evidence of increased oxidative stress and cell damage under hypoxia. Thus, the present findings show that the projected end-of-the-century deoxygenation levels elicit neglectable biological effects on shark embryos. On the other hand, hypoxia causes a high embryo mortality rate. Additionally, hypoxia makes embryos more vulnerable to predators, because the increased tail beat frequency will enhance the release of chemical and physical cues that can be detected by predators. The shortening of the shark freeze response under hypoxia also makes the embryos more prone to predation.pt_PT
dc.description.sponsorshipFCT AGA-KHAN/541746579/2019; LISBOA-01-0145-FEDER-028609; DL57/2016/CP1479/CT0023; LA/P/0069/2020; 2021.01030.CEECINDpt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.doi10.3390/biology12040577pt_PT
dc.identifier.eissn2079-7737
dc.identifier.urihttp://hdl.handle.net/10400.1/19644
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherMDPIpt_PT
dc.relationMultigenerational adaptation of ascidians to ocean warming and acidification
dc.relationOntogeny and ecological role of unsophisticated cognition of cleaner fishes in a changing ocean
dc.relationMarine and Environmental Sciences Centre
dc.relationApplied Molecular Biosciences Unit
dc.relationalterado para: “Immune and neuroendocrine responses of sharks to anthropogenic pressures” Immune and neuroendocrine response to climate change of teleost and cartilaginous fish
dc.relationalterado para: “Sharks in a changing ocean: a multiscale assessment of anthropogenic pressures on key marine predators”, Sharks Sixth Sense in a Changing Ocean - Effects of Ocean Warming and Acidification on Sharks Electroreception Sixth Sense in a Changing Ocean - Effects of Ocean Warming and Acidification on Sharks Electroreception
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.subjectClimate changept_PT
dc.subjectOxygen losspt_PT
dc.subjectElasmobranchpt_PT
dc.subjectEmbryogenesispt_PT
dc.subjectPredationpt_PT
dc.subjectSharkspt_PT
dc.titleImpacts of deoxygenation and hypoxia on shark embryos anti-predator behavior and oxidative stresspt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleMultigenerational adaptation of ascidians to ocean warming and acidification
oaire.awardTitleOntogeny and ecological role of unsophisticated cognition of cleaner fishes in a changing ocean
oaire.awardTitleMarine and Environmental Sciences Centre
oaire.awardTitleApplied Molecular Biosciences Unit
oaire.awardTitlealterado para: “Immune and neuroendocrine responses of sharks to anthropogenic pressures” Immune and neuroendocrine response to climate change of teleost and cartilaginous fish
oaire.awardTitlealterado para: “Sharks in a changing ocean: a multiscale assessment of anthropogenic pressures on key marine predators”, Sharks Sixth Sense in a Changing Ocean - Effects of Ocean Warming and Acidification on Sharks Electroreception Sixth Sense in a Changing Ocean - Effects of Ocean Warming and Acidification on Sharks Electroreception
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/9471 - RIDTI/PTDC%2FBIA-BMA%2F28609%2F2017/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/CEEC IND4ed/2021.01030.CEECIND%2FCP1654%2FCT0003/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDB%2F04292%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDP%2F04378%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/OE/SFRH%2FBD%2F145276%2F2019/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT//SFRH%2FBD%2F117890%2F2016/PT
oaire.citation.issue4pt_PT
oaire.citation.startPage577pt_PT
oaire.citation.titleBiologypt_PT
oaire.citation.volume12pt_PT
oaire.fundingStream9471 - RIDTI
oaire.fundingStreamCEEC IND4ed
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStreamOE
person.familyNameMartins Rebocho
person.givenNameSandra
person.identifier.orcid0000-0002-4755-9181
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
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