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Toxicity Reference Values for Chlorophacinone and Their Application for Assessing Anticoagulant Rodenticide Risk to Raptors

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Toxicity Reference Values for Chlorophacinone and Their Application for Assessing Anticoagulant Rodenticide Risk to Raptors University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln USGS Staff -- Published Research US Geological Survey 2015 Toxicity reference values for chlorophacinone and their application for assessing anticoagulant rodenticide risk to raptors Barnett A. Rattner United States Geological Survey, [email protected] Katherine E. Horak U.S. Department of Agriculture, [email protected] Rebecca S. Lazarus U.S. Geological Survey Sandra L. Schultz U.S. Geological Survey Susan Knowles U.S. Geological Survey See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/usgsstaffpub Part of the Geology Commons, Oceanography and Atmospheric Sciences and Meteorology Commons, Other Earth Sciences Commons, and the Other Environmental Sciences Commons Rattner, Barnett A.; Horak, Katherine E.; Lazarus, Rebecca S.; Schultz, Sandra L.; Knowles, Susan; Abbo, Benjamin G.; and Volker, Steven F., "Toxicity reference values for chlorophacinone and their application for assessing anticoagulant rodenticide risk to raptors" (2015). USGS Staff -- Published Research. 956. https://digitalcommons.unl.edu/usgsstaffpub/956 This Article is brought to you for free and open access by the US Geological Survey at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USGS Staff -- Published Research by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Barnett A. Rattner, Katherine E. Horak, Rebecca S. Lazarus, Sandra L. Schultz, Susan Knowles, Benjamin G. Abbo, and Steven F. Volker This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ usgsstaffpub/956 Ecotoxicology (2015) 24:720–734 DOI 10.1007/s10646-015-1418-8 Toxicity reference values for chlorophacinone and their application for assessing anticoagulant rodenticide risk to raptors Barnett A. Rattner • Katherine E. Horak • Rebecca S. Lazarus • Sandra L. Schultz • Susan Knowles • Benjamin G. Abbo • Steven F. Volker Accepted: 6 January 2015 / Published online: 20 January 2015 Ó Springer Science+Business Media New York (outside the USA) 2015 Abstract Despite widespread use and benefit, there are levels, and most frequently observed in pectoral muscle growing concerns regarding hazards of second-generation and heart. There were no apparent differences in toxicity anticoagulant rodenticides to non-target wildlife which between mechanically-amended and biologically-incorpo- may result in expanded use of first-generation compounds, rated CPN diet formulations. Dietary-based toxicity refer- including chlorophacinone (CPN). The toxicity of CPN ence values at which clotting times were prolonged in over a 7-day exposure period was investigated in American 50 % of the kestrels were 79.2 lg CPN consumed/kg body kestrels (Falco sparverius) fed either rat tissue mechani- weight-day for PT and 39.1 lg/kg body weight-day for cally-amended with CPN, tissue from rats fed RozolÒ bait RVVT. Based upon daily food consumption of kestrels and (biologically-incorporated CPN), or control diets (tissue previously reported CPN concentrations found in small from untreated rats or commercial bird of prey diet) mammals following field baiting trials, these toxicity ref- ad libitum. Nominal CPN concentrations in the formulated erence values might be exceeded by free-ranging raptors diets were 0.15, 0.75 and 1.5 lg/g food wet weight, and consuming such exposed prey. Tissue-based toxicity ref- measured concentrations averaged 94 % of target values. erence values for coagulopathy in 50 % of exposed birds Kestrel food consumption was similar among groups and were 0.107 lg CPN/g liver wet weight for PT and body weight varied by less than 6 %. Overt signs of 0.076 lg/g liver for RVVT, and are below the range of intoxication, liver CPN residues, and changes in pro- residue levels reported in raptor mortality incidents thrombin time (PT), Russell’s viper venom time (RVVT) attributed to CPN exposure. Sublethal responses associated and hematocrit, were generally dose-dependent. Histolog- with exposure to environmentally realistic concentrations ical evidence of hemorrhage was present at all CPN dose of CPN could compromise survival of free-ranging raptors, and should be considered in weighing the costs and benefits of anticoagulant rodenticide use in pest control and eradi- Electronic supplementary material The online version of this article (doi:10.1007/s10646-015-1418-8) contains supplementary cation programs. material, which is available to authorized users. Keywords American kestrel Á Anticoagulant & B. A. Rattner ( ) Á R. S. Lazarus Á S. L. Schultz rodenticide Á Birds Á Clotting time Á Non-target effects Á U.S. Geological Survey, Patuxent Wildlife Research Center, BARC East-Building 308, 10300 Baltimore Avenue, Beltsville, Risk assessment Á Secondary poisoning MD 20705, USA e-mail: [email protected] Introduction K. E. Horak Á B. G. Abbo Á S. F. Volker U.S. Department of Agriculture, Animal and Plant Health Inspection Service, National Wildlife Research Center, The control of commensal vertebrate pests in agricultural, Fort Collins, CO 80521, USA suburban and urban settings has been dependent on the use of anticoagulant rodenticides (ARs) for over 50 years. S. Knowles U.S. Geological Survey, National Wildlife Health Center, Second-generation ARs (principally brodifacoum) have Madison, WI 53711, USA played a central role in the eradication of invasive 123 Chlorophacinone and American kestrels 721 vertebrate pests in more than 700 island ecosystem resto- In the present study, we examined the toxicity of CPN in ration projects during the past 30 years (Howald et al. American kestrels (Falco sparverius), a species often 2007; Island Conservation 2012). Many reports describe selected as a model for raptorial birds (reviewed in Bardo exposure and unintentional mortality of birds and mam- and Bird 2009), and recently found to be considerably more mals (reviewed in Rattner et al. 2014b), although there is sensitive to the FGAR diphacinone than traditionally tested no definitive evidence of large-scale population declines in avian wildlife species (Northern bobwhite; mallards, Anas predatory and scavenging wildlife. It has been suggested platyrhynchos) (Rattner et al. 2011, 2012a, b). Graded that ARs are an additional mortality factor affecting pop- doses of CPN that had either been mechanically-amended ulations that are experiencing critical limitations (Brakes into rat tissue or biologically-incorporated into rat tissue and Smith 2005). In a probabilistic assessment of 270 were fed to kestrels, and measurements of food intake and raptors found dead, at least 11 % of the great horned owls tissue CPN residues were used to generate toxicity refer- (Bubo virginianus) analyzed were at risk of being directly ence values for coagulopathy and examine thresholds for killed by second-generation ARs (SGARs; bromadiolone, other toxicological effects. The inclusion of two dietary brodifacoum, difethialone) (Thomas et al. 2011). In much forms of CPN (i.e., mechanically-amended and biologi- of North America, the recent restrictions placed on the use cally-incorporated) was undertaken to address potential of SGARs (Health Canada 2012; USEPA 2012), are likely toxicological effects related to the presence of metabolites to result in expanded use of first-generation ARs (FGARs). and differences in bioavailability. With the likelihood that In Europe SGARs continue to be the mainstay of rodent FGAR use will continue, and perhaps even increase in the control (reviewed in Rattner et al. 2014b). near future, these and other data were incorporated into Chlorophacinone (CPN) is a FGAR that has been used assessments to more completely evaluate the risk of CPN worldwide for the control of commensal rodents, princi- to predatory birds. pally in agricultural and urban settings. It has been found in liver tissue of non-target birds in various monitoring and forensic investigations (Berny et al. 1997; Stone et al. Materials and methods 2003; Albert et al. 2010; Hughes et al. 2013; Vyas et al. 2013). There have been some secondary exposure incidents Animals in which the death of raptors (bald eagle Haliaeetus leu- cocephalus; barn owl Tyto alba; ferruginous hawk Buteo Procedures involving animals were reviewed and approved regalis; great horned owl) was attributed to CPN exposure by the Institutional Animal Care and Use Committees of (Berny et al. 1997; USEPA 2011a, 2012; USFWS 2012). the Patuxent Wildlife Research Center and the National Acute oral and short-term dietary toxicity studies in Wildlife Research Center. Adult 2- to 3-year old American Northern bobwhite (Colinus virginianus) in support of kestrels, propagated from the colony at Patuxent (Porter CPN registration categorize this FGAR as being moder- and Wiemeyer 1970), were transferred from flight pens to ately to highly toxic to birds (USEPA 2011a). Small-scale small cages (1.2 m long 9 0.8 m wide 9 0.6 m high) with studies with captive raptors fed CPN-exposed rodents have a shade roof, perches, food tray and water bowl. Only male described sublethal effects including hemorrhage, pro- birds were used, due in part to their availability from the longed clotting time (coagulopathy), and other signs of colony and potentially confounding effects of egg-laying in intoxication, but not mortality (Mendenhall and Pank 1980; reproductively active females. Individually housed kestrels Radvanyi et al. 1988; Riedel et al. 1988; Askham and
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