Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles

Handle URI:
http://hdl.handle.net/10754/622416
Title:
Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles
Authors:
Seibel, Brad A.; Schneider, Jillian L.; Kaartvedt, Stein ( 0000-0002-8793-2948 ) ; Wishner, Karen F.; Daly, Kendra L.
Abstract:
The effects of regional variations in oxygen and temperature levels with depth were assessed for the metabolism and hypoxia tolerance of dominant euphausiid species. The physiological strategies employed by these species facilitate prediction of changing vertical distributions with expanding oxygen minimum zones and inform estimates of the contribution of vertically migrating species to biogeochemical cycles. The migrating species from the Eastern Tropical Pacific (ETP), Euphausia eximia and Nematoscelis gracilis, tolerate a Partial Pressure (PO2) of 0.8 kPa at 10 °C (∼15 µM O2) for at least 12 h without mortality, while the California Current species, Nematoscelis difficilis, is incapable of surviving even 2.4 kPa PO2 (∼32 µM O2) for more than 3 h at that temperature. Euphausia diomedeae from the Red Sea migrates into an intermediate oxygen minimum zone, but one in which the temperature at depth remains near 22 °C. Euphausia diomedeae survived 1.6 kPa PO2 (∼22 µM O2) at 22 °C for the duration of six hour respiration experiments. Critical oxygen partial pressures were estimated for each species, and, for E. eximia, measured via oxygen consumption (2.1 kPa, 10 °C, n = 2) and lactate accumulation (1.1 kPa, 10 °C). A primary mechanism facilitating low oxygen tolerance is an ability to dramatically reduce energy expenditure during daytime forays into low oxygen waters. The ETP and Red Sea species reduced aerobic metabolism by more than 50% during exposure to hypoxia. Anaerobic glycolytic energy production, as indicated by whole-animal lactate accumulation, contributed only modestly to the energy deficit. Thus, the total metabolic rate was suppressed by ∼49–64%. Metabolic suppression during diel migrations to depth reduces the metabolic contribution of these species to vertical carbon and nitrogen flux (i.e., the biological pump) by an equivalent amount. Growing evidence suggests that metabolic suppression is a widespread strategy among migrating zooplankton in oxygen minimum zones and may have important implications for the economy and ecology of the oceans. The interacting effects of oxygen and temperature on the metabolism of oceanic species facilitate predictions of changing vertical distribution with climate change.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Seibel BA, Schneider JL, Kaartvedt S, Wishner KF, Daly KL (2016) Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles. Integrative and Comparative Biology 56: 510–523. Available: http://dx.doi.org/10.1093/icb/icw091.
Publisher:
Oxford University Press (OUP)
Journal:
Integrative and Comparative Biology
Issue Date:
10-Aug-2016
DOI:
10.1093/icb/icw091
Type:
Article
ISSN:
1540-7063; 1557-7023
Sponsors:
This project was funded by National Science Foundation grants (0852138 to B.A.S., 0526502 and 1459243 to B.A.S. and K.W., 0526545 to K.L.D.), and by the King Abdullah University of Science and Technology.
Additional Links:
http://icb.oxfordjournals.org/content/56/4/510
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorSeibel, Brad A.en
dc.contributor.authorSchneider, Jillian L.en
dc.contributor.authorKaartvedt, Steinen
dc.contributor.authorWishner, Karen F.en
dc.contributor.authorDaly, Kendra L.en
dc.date.accessioned2017-01-02T09:28:29Z-
dc.date.available2017-01-02T09:28:29Z-
dc.date.issued2016-08-10en
dc.identifier.citationSeibel BA, Schneider JL, Kaartvedt S, Wishner KF, Daly KL (2016) Hypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cycles. Integrative and Comparative Biology 56: 510–523. Available: http://dx.doi.org/10.1093/icb/icw091.en
dc.identifier.issn1540-7063en
dc.identifier.issn1557-7023en
dc.identifier.doi10.1093/icb/icw091en
dc.identifier.urihttp://hdl.handle.net/10754/622416-
dc.description.abstractThe effects of regional variations in oxygen and temperature levels with depth were assessed for the metabolism and hypoxia tolerance of dominant euphausiid species. The physiological strategies employed by these species facilitate prediction of changing vertical distributions with expanding oxygen minimum zones and inform estimates of the contribution of vertically migrating species to biogeochemical cycles. The migrating species from the Eastern Tropical Pacific (ETP), Euphausia eximia and Nematoscelis gracilis, tolerate a Partial Pressure (PO2) of 0.8 kPa at 10 °C (∼15 µM O2) for at least 12 h without mortality, while the California Current species, Nematoscelis difficilis, is incapable of surviving even 2.4 kPa PO2 (∼32 µM O2) for more than 3 h at that temperature. Euphausia diomedeae from the Red Sea migrates into an intermediate oxygen minimum zone, but one in which the temperature at depth remains near 22 °C. Euphausia diomedeae survived 1.6 kPa PO2 (∼22 µM O2) at 22 °C for the duration of six hour respiration experiments. Critical oxygen partial pressures were estimated for each species, and, for E. eximia, measured via oxygen consumption (2.1 kPa, 10 °C, n = 2) and lactate accumulation (1.1 kPa, 10 °C). A primary mechanism facilitating low oxygen tolerance is an ability to dramatically reduce energy expenditure during daytime forays into low oxygen waters. The ETP and Red Sea species reduced aerobic metabolism by more than 50% during exposure to hypoxia. Anaerobic glycolytic energy production, as indicated by whole-animal lactate accumulation, contributed only modestly to the energy deficit. Thus, the total metabolic rate was suppressed by ∼49–64%. Metabolic suppression during diel migrations to depth reduces the metabolic contribution of these species to vertical carbon and nitrogen flux (i.e., the biological pump) by an equivalent amount. Growing evidence suggests that metabolic suppression is a widespread strategy among migrating zooplankton in oxygen minimum zones and may have important implications for the economy and ecology of the oceans. The interacting effects of oxygen and temperature on the metabolism of oceanic species facilitate predictions of changing vertical distribution with climate change.en
dc.description.sponsorshipThis project was funded by National Science Foundation grants (0852138 to B.A.S., 0526502 and 1459243 to B.A.S. and K.W., 0526545 to K.L.D.), and by the King Abdullah University of Science and Technology.en
dc.publisherOxford University Press (OUP)en
dc.relation.urlhttp://icb.oxfordjournals.org/content/56/4/510en
dc.titleHypoxia Tolerance and Metabolic Suppression in Oxygen Minimum Zone Euphausiids: Implications for Ocean Deoxygenation and Biogeochemical Cyclesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalIntegrative and Comparative Biologyen
dc.contributor.institutionCollege of Marine Science, University of South Florida, St. Petersburg, FL 33701, USAen
dc.contributor.institutionPaul Cuffee School, 30 Barton St Providence, RI 02909, USAen
dc.contributor.institutionGraduate School of Oceanography, University of Rhode Island, Narragansett, RI, USAen
kaust.authorKaartvedt, Steinen
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