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      Anticoagulant rodenticide exposure and toxicosis in bald eagles ( Haliaeetus leucocephalus) and golden eagles ( Aquila chrysaetos) in the United States

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          Abstract

          Raptors, including eagles, are geographically widespread and sit atop the food chain, thereby serving an important role in maintaining ecosystem balance. After facing population declines associated with exposure to organochlorine insecticides such as dichlorodiphenyltrichloroethane (DDT), bald eagles ( Haliaeetus leucocephalus) have recovered from the brink of extinction. However, both bald and golden eagles ( Aquila chrysaetos) are exposed to a variety of other toxic compounds in the environment that could have population impacts. Few studies have focused on anticoagulant rodenticide (AR) exposure in eagles. Therefore, the purpose of this study was to determine the types of ARs that eagles are exposed to in the USA and better define the extent of toxicosis (i.e., fatal illness due to compound exposure). Diagnostic case records from bald and golden eagles submitted to the Southeastern Cooperative Wildlife Disease Study (University of Georgia) 2014 through 2018 were reviewed. Overall, 303 eagles were examined, and the livers from 116 bald eagles and 17 golden eagles were tested for ARs. The percentage of AR exposure (i.e., detectable levels but not associated with mortality) in eagles was high; ARs were detected in 109 (82%) eagles, including 96 (83%) bald eagles and 13 (77%) golden eagles. Anticoagulant rodenticide toxicosis was determined to be the cause of mortality in 12 (4%) of the 303 eagles examined, including 11 bald eagles and 1 golden eagle. Six different AR compounds were detected in these eagles, with brodifacoum and bromadiolone most frequently detected (81% and 25% of eagles tested, respectively). These results suggest that some ARs, most notably brodifacoum, are widespread in the environment and are commonly consumed by eagles. This highlights the need for research to understand the pathways of AR exposure in eagles, which may help inform policy and regulatory actions to mitigate AR exposure risk.

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          Most cited references39

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          Ban of DDT and subsequent recovery of Reproduction in bald eagles.

          Reproduction of bald eagles in northwestern Ontario declined from 1.26 young per breeding area in 1966 to a low of 0.46 in 1974 and then increased to 1.12 in 1981. Residues of DDE in addled eggs showed a significant inverse relation, confirming the effects of this toxicant on bald eagle reproduction at the population level and the effectiveness of the ban on DDT. The recovery from DDE contamination in bald eagles appears to be occurring much more rapidly than predicted.
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            Second generation anticoagulant rodenticides in predatory birds: Probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada.

            Second-generation anticoagulant rodenticides (SGARs) are widely used to control rodent pests but exposure and poisonings occur in non-target species, such as birds of prey. Liver residues are often analysed to detect exposure in birds found dead but their use to assess toxicity of SGARs is problematic. We analysed published data on hepatic rodenticide residues and associated symptoms of anticoagulant poisoning from 270 birds of prey using logistic regression to estimate the probability of toxicosis associated with different liver SGAR residues. We also evaluated exposure to SGARs on a national level in Canada by analysing 196 livers from great horned owls (Bubo virginianus) and red-tailed hawks (Buteo jamaicensis) found dead at locations across the country. Analysis of a broader sample of raptor species from Quebec also helped define the taxonomic breadth of contamination. Calculated probability curves suggest significant species differences in sensitivity to SGARs and significant likelihood of toxicosis below previously suggested concentrations of concern (<0.1mg/kg). Analysis of birds from Quebec showed that a broad range of raptor species are exposed to SGARs, indicating that generalised terrestrial food chains could be contaminated in the vicinity of the sampled areas. Of the two species for which we had samples from across Canada, great horned owls are exposed to SGARs to a greater extent than red-tailed hawks and the liver residue levels were also higher. Using our probability estimates of effect, we estimate that a minimum of 11% of the sampled great horned owl population is at risk of being directly killed by SGARs. This is the first time the potential mortality impact of SGARs on a raptor population has been estimated.
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              Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife.

              Despite a long history of successful use, routine application of some anticoagulant rodenticides (ARs) may be at a crossroad due to new regulatory guidelines intended to mitigate risk. An adverse outcome pathway for ARs was developed to identify information gaps and end points to assess the effectiveness of regulations. This framework describes chemical properties of ARs, established macromolecular interactions by inhibition of vitamin K epoxide reductase, cellular responses including altered clotting factor processing and coagulopathy, organ level effects such as hemorrhage, organism responses with linkages to reduced fitness and mortality, and potential consequences to predator populations. Risk assessments have led to restrictions affecting use of some second-generation ARs (SGARs) in North America. While the European regulatory community highlighted significant or unacceptable risk of ARs to nontarget wildlife, use of SGARs in most EU member states remains authorized due to public health concerns and the absence of safe alternatives. For purposes of conservation and restoration of island habitats, SGARs remain a mainstay for eradication of invasive species. There are significant data gaps related to exposure pathways, comparative species sensitivity, consequences of sublethal effects, potential hazards of greater AR residues in genetically resistant prey, effects of low-level exposure to multiple rodenticides, and quantitative data on the magnitude of nontarget wildlife mortality.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: 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
                7 April 2021
                2021
                : 16
                : 4
                : e0246134
                Affiliations
                [1 ] Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA, United States of America
                [2 ] United States Fish and Wildlife Service, National Wildlife Refuge System, Chiefland, FL, United States of America
                [3 ] Florida Fish and Wildlife Conservation Commission, Gainesville, FL, United States of America
                [4 ] Kentucky Department of Fish and Wildlife Resources, Frankfort, KY, United States of America
                [5 ] California Animal Health and Food Safety Laboratories, School of Veterinary Medicine, University of California, Davis, CA, United States of America
                [6 ] United States Fish and Wildlife Service, Division of Migratory Bird Management, Albuquerque, New MX, United States of America
                Universidade Federal de Minas Gerais, BRAZIL
                Author notes

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

                [¤a]

                Current address: School of Veterinary Medicine, University of California, Davis, CA, United States of America

                [¤b]

                Current address: School of Veterinary Medicine, Ross University, Basseterre, St. Kitts, West Indies

                [¤c]

                Current address: North Dakota Game and Fish Department, Bismarck, ND, United States of America

                [¤d]

                Current address: Mississippi Veterinary and Research Diagnostic Laboratory, College of Veterinary Medicine, Mississippi State University, Pearl, MI, United States of America

                [¤e]

                Current address: Wisconsin Veterinary Diagnostic Laboratory, University of Wisconsin, Madison, WI, United States of America

                ‡ These authors also contributed equally to this work.

                Author information
                https://orcid.org/0000-0001-5931-175X
                https://orcid.org/0000-0002-2161-6491
                Article
                PONE-D-20-19740
                10.1371/journal.pone.0246134
                8026043
                33826627
                fa998fd2-eabd-4b1c-a935-df09c6f24a8d

                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
                : 26 June 2020
                : 13 January 2021
                Page count
                Figures: 3, Tables: 3, Pages: 13
                Funding
                Funded by: The State Wildlife Management Agencies of SCWDS
                Funded by: The United States Fish and Wildlife Service National Wildlife Refuge System, United States Department of Interior
                Award ID: F15PX01848
                Funded by: The United States Geological Survey Ecosystems Mission Area, United States Department of Interior
                Award ID: G18AC00319
                We are grateful for funding provided by member state wildlife management agencies of SCWDS in Alabama, Arkansas, Florida, Georgia, Kentucky, Kansas, Louisiana, Maryland, Mississippi, Missouri, Nebraska, North Carolina, Oklahoma, Pennsylvania, South Carolina, Tennessee, Virginia, and West Virginia provided by the Federal Aid to Wildlife Restoration Act (50 Stat.917). Further, we thank our partnering federal agencies, including the United States Fish and Wildlife Service National Wildlife Refuge System, United States Department of Interior (F15PX01848) and the United States Geological Survey Ecosystems Mission Area, United States Department of Interior (G18AC00319). The funders had no role in study design, data collection and data analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Raptors
                Eagles
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Birds
                Raptors
                Eagles
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Wildlife
                Biology and Life Sciences
                Zoology
                Animals
                Wildlife
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Raptors
                Owls
                Biology and Life Sciences
                Zoology
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                Vertebrates
                Amniotes
                Birds
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                Owls
                Biology and Life Sciences
                Organisms
                Eukaryota
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                Biology and Life Sciences
                Zoology
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                Biology and Life Sciences
                Veterinary Science
                Veterinary Medicine
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                Eukaryota
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                Vertebrates
                Amniotes
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                Biology and Life Sciences
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