{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T06:20:25Z","timestamp":1791526825786,"version":"4.3.4"},"reference-count":39,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T00:00:00Z","timestamp":1617753600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"name":"The State Wildlife Management Agencies of SCWDS"},{"name":"The United States Fish and Wildlife Service National Wildlife Refuge System, United States Department of Interior","award":["F15PX01848"],"award-info":[{"award-number":["F15PX01848"]}]},{"name":"The United States Geological Survey Ecosystems Mission Area, United States Department of Interior","award":["G18AC00319"],"award-info":[{"award-number":["G18AC00319"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>\n                    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 (\n                    <jats:italic>Haliaeetus leucocephalus<\/jats:italic>\n                    ) have recovered from the brink of extinction. However, both bald and golden eagles (\n                    <jats:italic>Aquila chrysaetos<\/jats:italic>\n                    ) 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.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0246134","type":"journal-article","created":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T13:56:57Z","timestamp":1617803817000},"page":"e0246134","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":36,"title":["Anticoagulant rodenticide exposure and toxicosis in bald eagles (Haliaeetus leucocephalus) and golden eagles (Aquila chrysaetos) in the United States"],"prefix":"10.1371","volume":"16","author":[{"given":"Kevin D.","family":"Niedringhaus","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5931-175X","authenticated-orcid":true,"given":"Nicole M.","family":"Nemeth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha","family":"Gibbs","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jared","family":"Zimmerman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Shender","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kate","family":"Slankard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heather","family":"Fenton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bahnson","family":"Charlie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martha Frances","family":"Dalton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth J.","family":"Elsmo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Poppenga","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian","family":"Millsap","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2161-6491","authenticated-orcid":true,"given":"Mark G.","family":"Ruder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,4,7]]},"reference":[{"key":"pone.0246134.ref001","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.1126\/science.7146905","article-title":"Ban of DDT and subsequent recovery of reproduction in bald eagles","volume":"218","author":"JW Grier","year":"1982","journal-title":"Science"},{"key":"pone.0246134.ref002","doi-asserted-by":"crossref","first-page":"1436","DOI":"10.1002\/jwmg.588","article-title":"Golden eagle population trends in the western United States: 1968\u20132010","volume":"77","author":"BA Millsap","year":"2013","journal-title":"J Wildl Manag"},{"key":"pone.0246134.ref003","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0006-3207(97)00051-7","article-title":"Population status and recent trends in Canadian raptors: a review","volume":"83","author":"DA Kirk","year":"1998","journal-title":"Biol Conserv"},{"key":"pone.0246134.ref004","volume-title":"Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. Office of Prevention, Pesticides, and Toxic Substances. Office of Pesticides Programs, Environmental Fate and Effects Division.","author":"W Erickson","year":"2004"},{"key":"pone.0246134.ref005","doi-asserted-by":"crossref","first-page":"273","DOI":"10.3356\/JRR-16-19.1","article-title":"Characterizing golden eagle risk to lead and antico-agulant rodenticide exposure: a review","volume":"51","author":"G Herring","year":"2017","journal-title":"J Raptor Res"},{"key":"pone.0246134.ref006","doi-asserted-by":"crossref","first-page":"8433","DOI":"10.1021\/es501740n","article-title":"Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife","volume":"48","author":"BA Rattner","year":"2014","journal-title":"Environ Sci Tech"},{"key":"pone.0246134.ref007","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1159\/000137881","article-title":"Dispositional pharmacodynamics characteristics of brodifacoum in warfarin-sensitive rats","volume":"27","author":"KA Bachmann","year":"1983","journal-title":"Pharmacology"},{"key":"pone.0246134.ref008","doi-asserted-by":"crossref","first-page":"187","DOI":"10.7589\/0090-3558-35.2.187","article-title":"Poisoning of wildlife with anticoagulant rodenticides in New York","volume":"35","author":"WB Stone","year":"1999","journal-title":"J Wildl Dis"},{"key":"pone.0246134.ref009","unstructured":"US Environmental Protection Agency (2008). Rodenticides Final Risk Mitigation Decision. Federal register: The Daily Journal of the US Government, 73 FR 31868, pp 31868\u201331869. https:\/\/www.federalregister.gov\/documents\/2008\/06\/04\/E8-12493\/rodenticides-final-risk-mitigation-decision-notice-of-availability. Accessed October 18, 2019."},{"key":"pone.0246134.ref010","unstructured":"US Environmental Protection Agency, (2014). Product Cancellation Order for Certain Rodenticide Registrations. Federal Register: The Daily Journal of the US Government, 79 FR 45802, pp 45802\u201345803. https:\/\/www.federalregister.gov\/documents\/2014\/08\/06\/2014-18361\/product-cancellation-order-for-certain-rodenticide-registrations. Accessed October 18, 2019."},{"key":"pone.0246134.ref011","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1007\/s10661-013-3422-x","article-title":"Exposure pathways of anticoagulant rodenticides to nontarget wildlife","volume":"186","author":"JE Elliott","year":"2014","journal-title":"Environ Monit Assess"},{"issue":"11","key":"pone.0246134.ref012","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1002\/etc.4853","article-title":"Continued anticoagulant rodenticide exposure of red-tailed hawks (Buteo jamaicensis) in the Northeastern United States with an evaluation of serum for biomonitoring.","volume":"39","author":"M Murray","year":"2020","journal-title":"Environ Toxicol Chem"},{"key":"pone.0246134.ref013","first-page":"311","article-title":"Secondary poisoning of owls by anticoagulant rodenticides","volume":"8","author":"VM Mendenhall","year":"1980","journal-title":"Wildl Soc Bull"},{"key":"pone.0246134.ref014","first-page":"219","article-title":"Secondary and tertiary poisoning risks associated with brodifacoum.","volume":"23","author":"CT Eason","year":"1999","journal-title":"N Z J Ecol"},{"key":"pone.0246134.ref015","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1016\/j.envint.2011.03.010","article-title":"Second generation anticoagulant rodenticides in predatory birds: probabilistic characterization of toxic liver concentrations and implications for predatory bird populations in Canada.","volume":"37","author":"P Thomas","year":"2011","journal-title":"Environ Int"},{"key":"pone.0246134.ref016","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1007\/s00244-012-9771-6","article-title":"High exposure rates of anticoagulant rodenticides in predatory bird species in intensively managed landscapes in Denmark","volume":"63","author":"T Christensen","year":"2012","journal-title":"Arch Environ Contam Toxicol"},{"key":"pone.0246134.ref017","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1638\/2010-0188.1","article-title":"Anticoagulant rodenticide exposure and toxicosis in four species of birds of prey presented to a wildlife clinic in Massachusetts, 2006\u20132010","volume":"42","author":"M Murray","year":"2011","journal-title":"J Zoo Wildl Med"},{"key":"pone.0246134.ref018","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1007\/s00128-013-1135-z","article-title":"Anticoagulant rodenticides in red-tailed hawks, Buteo jamaicensis, and great horned owls, Bubo virginianus, from New Jersey, USA, 2008\u20132010","volume":"92","author":"W Stansley","year":"2014","journal-title":"Bull Environ Cont Toxicol"},{"key":"pone.0246134.ref019","doi-asserted-by":"crossref","first-page":"6682","DOI":"10.1021\/acs.jafc.7b02280","article-title":"Development and val-idation of quantitative ultraperformance liquid chromatography-tandem mass spectrometry assay for anticoagulant rodenticides in liver","volume":"65","author":"LL Smith","year":"2017","journal-title":"J Agric Food Chem"},{"key":"pone.0246134.ref020","doi-asserted-by":"crossref","first-page":"92","DOI":"10.7589\/0090-3558-42.1.92","article-title":"Wild bird mortality and West Nile virus surveillance: biases associated with detection, reporting, and carcass persistence","volume":"42","author":"MR Ward","year":"2006","journal-title":"J Wildl Dis"},{"key":"pone.0246134.ref021","first-page":"200","article-title":"Assessing individual and population-level effects of anticoagulant rodenticides on wildlife","volume":"13","author":"N Quinn","year":"2019","journal-title":"Hum-Wild Interact"},{"key":"pone.0246134.ref022","first-page":"228","volume-title":"Anticoagulant Rodenticides and Wildlife.","author":"S Hindmarch","year":"2018"},{"key":"pone.0246134.ref023","first-page":"8","article-title":"Mortality, morbidity, and lead poisoning of eagles in Western Canada, 1986\u20131998","volume":"37","author":"M Wayland","year":"2003","journal-title":"J Raptor Res"},{"key":"pone.0246134.ref024","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1638\/05-099.1","article-title":"Morbidity and mortality of bald eagles (Haliaeetus leucocepha-lus) and peregrine falcons (Falco peregrinus) admitted to the Wildlife Center of Virginia, 1993\u20132003.","volume":"38","author":"MC Harris","year":"2007","journal-title":"J Zoo Wildl Med"},{"key":"pone.0246134.ref025","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1002\/wsb.469","article-title":"Causes of mortality in eagles submitted to the National Wildlife Health Center 1975\u20132013","volume":"38","author":"RE Russell","year":"2014","journal-title":"Wildl Soc Bull"},{"key":"pone.0246134.ref026","doi-asserted-by":"crossref","unstructured":"Hosea R. 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Office of Prevention, Pesticides, and Toxic Substances.","author":"S Bradbury","year":"2008"},{"issue":"2","key":"pone.0246134.ref036","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1002\/ps.6137","article-title":"Challenges in the interpretation of anticoagulant rodenticide residues and toxicity in predatory and scavenging birds","volume":"77","author":"BA Rattner","year":"2021","journal-title":"Pest Manag Sci"},{"key":"pone.0246134.ref037","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1016\/j.scitotenv.2018.11.485","article-title":"Use of blood clotting assays to assess potential anti-coagulant rodenticide exposure and effects in free-ranging birds of prey","volume":"657","author":"S Hindmarch","year":"2019","journal-title":"Sci Total Environ"},{"key":"pone.0246134.ref038","doi-asserted-by":"crossref","first-page":"4729","DOI":"10.1016\/j.scitotenv.2011.07.007","article-title":"Side effects of rodent control on non-target species: rodenticides increase parasite and pathogen burden in great bustards","volume":"409","author":"JA Lemus","year":"2011","journal-title":"Sci Total Environ"},{"key":"pone.0246134.ref039","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1002\/ps.4435","article-title":"A negative association between bromadiolone exposure and nestling body condition in common kestrels: management implications for vole outbreaks","volume":"73","author":"J Mart\u00ednez-Padilla","year":"2016","journal-title":"Pest Manag Sci"}],"updated-by":[{"DOI":"10.1371\/journal.pone.0328387","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2025,7,15]],"date-time":"2025-07-15T00:00:00Z","timestamp":1752537600000}}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0246134","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,7]],"date-time":"2021-04-07T13:57:44Z","timestamp":1617803864000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0246134"}},"subtitle":[],"editor":[{"given":"Benito","family":"Soto-Blanco","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,4,7]]},"references-count":39,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4,7]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0246134","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,7]]}}}