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      Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016

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          Abstract

          About 62,000 dead or dying common murres ( Uria aalge), the trophically dominant fish-eating seabird of the North Pacific, washed ashore between summer 2015 and spring 2016 on beaches from California to Alaska. Most birds were severely emaciated and, so far, no evidence for anything other than starvation was found to explain this mass mortality. Three-quarters of murres were found in the Gulf of Alaska and the remainder along the West Coast. Studies show that only a fraction of birds that die at sea typically wash ashore, and we estimate that total mortality approached 1 million birds. About two-thirds of murres killed were adults, a substantial blow to breeding populations. Additionally, 22 complete reproductive failures were observed at multiple colonies region-wide during (2015) and after (2016–2017) the mass mortality event. Die-offs and breeding failures occur sporadically in murres, but the magnitude, duration and spatial extent of this die-off, associated with multi-colony and multi-year reproductive failures, is unprecedented and astonishing. These events co-occurred with the most powerful marine heatwave on record that persisted through 2014–2016 and created an enormous volume of ocean water (the “Blob”) from California to Alaska with temperatures that exceeded average by 2–3 standard deviations. Other studies indicate that this prolonged heatwave reduced phytoplankton biomass and restructured zooplankton communities in favor of lower-calorie species, while it simultaneously increased metabolically driven food demands of ectothermic forage fish. In response, forage fish quality and quantity diminished. Similarly, large ectothermic groundfish were thought to have increased their demand for forage fish, resulting in greater top-predator demands for diminished forage fish resources. We hypothesize that these bottom-up and top-down forces created an “ectothermic vise” on forage species leading to their system-wide scarcity and resulting in mass mortality of murres and many other fish, bird and mammal species in the region during 2014–2017.

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          A hierarchical approach to defining marine heatwaves

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            Marine heatwaves under global warming

            Marine heatwaves (MHWs) are periods of extreme warm sea surface temperature that persist for days to months1 and can extend up to thousands of kilometres2. Some of the recently observed marine heatwaves revealed the high vulnerability of marine ecosystems3-11 and fisheries12-14 to such extreme climate events. Yet our knowledge about past occurrences15 and the future progression of MHWs is very limited. Here we use satellite observations and a suite of Earth system model simulations to show that MHWs have already become longer-lasting and more frequent, extensive and intense in the past few decades, and that this trend will accelerate under further global warming. Between 1982 and 2016, we detect a doubling in the number of MHW days, and this number is projected to further increase on average by a factor of 16 for global warming of 1.5 degrees Celsius relative to preindustrial levels and by a factor of 23 for global warming of 2.0 degrees Celsius. However, current national policies for the reduction of global carbon emissions are predicted to result in global warming of about 3.5 degrees Celsius by the end of the twenty-first century16, for which models project an average increase in the probability of MHWs by a factor of 41. At this level of warming, MHWs have an average spatial extent that is 21 times bigger than in preindustrial times, last on average 112 days and reach maximum sea surface temperature anomaly intensities of 2.5 degrees Celsius. The largest changes are projected to occur in the western tropical Pacific and Arctic oceans. Today, 87 per cent of MHWs are attributable to human-induced warming, with this ratio increasing to nearly 100 per cent under any global warming scenario exceeding 2 degrees Celsius. Our results suggest that MHWs will become very frequent and extreme under global warming, probably pushing marine organisms and ecosystems to the limits of their resilience and even beyond, which could cause irreversible changes.
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              Causes and impacts of the 2014 warm anomaly in the NE Pacific

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                15 January 2020
                2020
                : 15
                : 1
                : e0226087
                Affiliations
                [1 ] U.S. Geological Survey, Alaska Science Center, Anchorage, Alaska, United States of America
                [2 ] University of Washington, School of Aquatic and Fishery Sciences, COASST, Seattle, Washington, United States of America
                [3 ] U.S. Fish and Wildlife Service, Alaska Maritime National Wildlife Refuge, Homer, Alaska, United States of America
                [4 ] U.S. Geological Survey, Alaska Science Center, Juneau, Alaska, United States of America
                [5 ] U.S. Fish and Wildlife Service, Migratory Bird Management, Anchorage, Alaska, United States of America
                [6 ] U.S. Geological Survey, National Wildlife Health Center, Madison, Wisconsin, United States of America
                [7 ] Farallon Institute, Petaluma, California, United States of America
                [8 ] International Bird Rescue, San Francisco Bay Center, Fairfield, California, United States of America
                [9 ] U.S. Fish and Wildlife Service, Kodiak National Wildlife Refuge, Kodiak, Alaska, United States of America
                [10 ] U.S. Fish and Wildlife Service, San Francisco Bay National Wildlife Refuge Complex, Fremont, California, United States of America
                [11 ] Department of Wildlife, Humboldt State University, Arcata, California, United States of America
                [12 ] National Park Service, Fairbanks, Alaska, United States of America
                [13 ] NOAA Fisheries, Alaska Fisheries Science Center, Auk Bay Laboratories, Ted Stevens Marine Research Institute, Juneau, Alaska, United States of America
                [14 ] Moss Landing Marine Laboratories, BeachCOMBERS, Moss Landing, California, United States of America
                [15 ] NOAA Greater Farallones National Marine Sanctuary, Beach Watch, San Francisco, California, United States of America
                [16 ] Point Blue Conservation Science, Petaluma, CA, United States of America
                Hawaii Pacific University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-4417-5748
                http://orcid.org/0000-0002-2560-4148
                Article
                PONE-D-19-19863
                10.1371/journal.pone.0226087
                6961838
                31940310
                f8002216-1b73-49e6-a99d-c4620afe3f26

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 14 July 2019
                : 18 November 2019
                Page count
                Figures: 6, Tables: 1, Pages: 32
                Funding
                Funded by: NSF EHR/DRL
                Award ID: 1322820
                Award Recipient :
                Funded by: Washington Department of Fish and Wildlife
                Award ID: 13-1435
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100012635, North Pacific Research Board;
                Award Recipient :
                These analyses were supported by funding from the USGS Ecosystems Mission Area and the North Pacific Research board to JFP; and by NSF EHR/DRL award 1322820 and Washington Department of Fish and Wildlife award 13-1435 to JKP, and NPS Ocean Alaska Science and Learning Center grant to HAC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Beaches
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Marine Fish
                Biology and Life Sciences
                Marine Biology
                Marine Fish
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Marine Fish
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Death Rates
                People and places
                Geographical locations
                North America
                United States
                Alaska
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Earth sciences
                Marine and aquatic sciences
                Bodies of water
                Gulfs
                Gulf of Alaska
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information Files, with the exception of data found elsewhere: Beach survey and necropsy data from studies conducted by the USGS Alaska Science Center (DOI: https://doi.org/10.5066/P9E8RE9I); pathology/necropsy data from the USGS National Wildlife Health Center (DOI: https://doi.org/10.5066/P9O4Y5EO); Beach survey data available from COASST ( www.COASST.org), BeachCOMBERS ( https://data.cencoos.org), and Beach Watch ( www.farallones.org/BeachData/BeachWatchData.php), raw data requests at COASST@ 123456uw.edu , jharvey@ 123456mlml.calstate.edu , jan.roletto@ 123456noaa.gov , respectively, with data use agreement. Murre breeding biology data are available upon request from the U.S. Fish and Wildlife Service National Wildlife Refuges (NWR) ( https://www.fws.gov/refuges/) including San Francisco Bay NWR Complex, Castle Rock NWR, Oregon Coastal NWR Complex, and the Alaska Maritime NWR, and from Pointblue Conservation Science ( jjahncke@ 123456pointblue.org ). Data on pelagic distribution of murres in Supporting Information were from the USGS North Pacific Pelagic Seabird Database (NPPSD) ( https://doi.org/10.5066/F7WQ01T3). Data on sea surface temperatures were from the Hadley Center Sea Ice and Sea Surface Temperature (HadISST) data set freely available at ( https://www.metoffice.gov.uk/hadobs/hadisst/).

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