Rodenticide Incidents of Exposure and Adverse Effects on Non-Raptor Birds

Science of the Total Environment 609 (2017) 68–76

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Rodenticide incidents of exposure and adverse effects on non-raptor birds

Nimish B. Vyas

U.S·Geological Survey, Patuxent Wildlife Research Center, Beltsville Lab, BARC-East, Building 308, 10300 Baltimore Avenue, Beltsville, Maryland 20705, USA article info abstract

Article history: Interest in the adverse effects of rodenticides on birds has focused primarily on raptors. However, non-raptor Received 3 April 2017 birds are also poisoned (rodenticide exposure resulting in adverse effects including mortality) by rodenticides Received in revised form 29 June 2017 through consumption of the rodenticide bait and contaminated prey. A literature search for rodenticide incidents Accepted 1 July 2017 (evidence of exposure to a rodenticide, adverse effects, or exposure to placebo baits) involving non-raptor birds Available online xxxx returned 641 records spanning the years 1931 to 2016. The incidents included 17 orders, 58 families, and 190 Editor: D. Barcelo non-raptor bird species. Nineteen anticoagulant and non-anticoagulant rodenticide active ingredients were associated with the incidents. The number of incidents and species detected were compared by surveillance method. An incident was considered to have been reported through passive surveillance if it was voluntarily reported to the authorities whereas the report of an incident found through ﬁeld work that was conducted with the objective of documenting adverse effects on birds was determined to be from active surveillance. More incidents were reported from passive surveillance than with active surveillance but a signiﬁcantly greater number of species were detected in proportion to the number of incidents found through active surveillance than with passive surveillance (z = 7.61, p b 0.01). Results suggest that reliance on only one surveillance method can underestimate the number of incidents that have occurred and the number of species that are affected. Although rodenticides are used worldwide, incident records were found from only 15 countries. Therefore, awareness of the breadth of species diversity of non-raptor bird poisonings from rodenticides may increase incident reportings and can strengthen the predictions of harm characterized by risk assessments. Published by Elsevier B.V.

1. Introduction (https://www.epa.gov/pesticide-incidents/introduction-pesticide- incidents). Hereafter I use the term ‘incident’ to also include ingestion of Rodenticides are used worldwide to protect agriculture, human placebo baits that were applied using operational application tech- health, and ecosystems from a variety of mammalian pests (Eason et niques. Placebo bait trials have been used to predict the risks to non-tar- al., 2015; United States Environmental Protection Agency, US EPA, get birds that may occur from rodenticide applications (e.g. McClelland, 2008). Rodenticides are broad-spectrum vertebrate control agents and 2002; Sztukowski and Kesler, 2013; Torr, 2002). I included placebo bait therefore they are also hazardous to birds. Monitoring for rodenticide exposures as incidents because the actual hazards to birds following ro- exposure and adverse effects on birds has generally focused on raptors denticide applications may exceed the risks predicted by the placebo (e.g. Christensen et al., 2012; Gómez-Ramírez et al., 2014; Thomas et bait trials and because rodenticide applications may be conducted de- al., 2011; Walker et al., 2015). However non-raptor bird mortalities spite observations of birds feeding on the placebo bait because the have occurred from feeding on rodenticide bait (primary exposure) risks are considered to be acceptable with respect to the long-term ben- and via secondary exposure through consumption of contaminated efits of the rodenticide application (e.g. Empson and Miskelly, 1999; prey (Berny et al., 1997; Sánchez-Barbudo et al., 2012; Spurr, 1994; McIlroy and Gifford, 1991). Vyas et al., 2013). Traditionally, the term ‘incident’ has been defined as Incident data provide insight into the hazards of rodenticides follow- an adverse effect (e.g. http://www.hc-sc.gc.ca/cps-spc/pest/part/ ing operational applications. Below I summarize rodenticide incidents protect-proteger/incident/index-eng.php). Recently, the US EPA ex- of non-raptor bird species from literature spanning 1931–2016; provide panded this definition to include pesticide exposure or an adverse effect an overview of the anthropogenic, abiotic, and biotic factors that contribute to rodenticide exposure and poisoning; and discuss the influence of active and passive surveillance methods on documenting the E-mail address: [email protected]. incidents. The overall objective of this paper is to increase awareness

http://dx.doi.org/10.1016/j.scitotenv.2017.07.004 0048-9697/Published by Elsevier B.V. N.B. Vyas / Science of the Total Environment 609 (2017) 68–76 69 of the breadth of rodenticide exposure and adverse effects to non-raptor Rodenticide applications specifically purposed for habitat and spe- birds. Knowledge that rodenticides are hazardous to non-raptor birds cies conservation (e.g. (e.g. for eradicating invasive non-target mam- can benefit their conservation by encouraging conscientious compli- mals on islands, Eason et al., 2015) were categorized as applications ance with the rodenticide label; increasing incident reporting by the for ecological restoration. The non-raptor bird incident records that ei- public; improving or establishing incident monitoring schemes that in- ther stated or reasonably implied that rodenticide applications were clude non-raptor birds; establishing or improving infrastructure for sur- conducted for human enterprises (e.g. agriculture, see Bildfell et al., veillance of non-raptor bird incidents, determination of their causality, 2013) were considered to be applications for human welfare. In some and release of incident records for public access; clarifying routes of ro- cases, operational rodenticide applications were conducted to deter- denticide exposure to raptors (Elliott et al., 2016); and by supporting mine their risks to birds (e.g. Elliott et al., 2014; McIlroy and Gifford, the predictions of harm characterized by risk assessments. 1991; Ramey and Sterner, 1995). These applications were considered to have been conducted for human welfare because although the studies focused on bird exposure and adverse effects, the applications mim- 2. Methods icked those that are operationally conducted for human welfare and not for ecological restoration. 2.1. Literature search 2.2. Data analysis Iusedtheterms‘rodenticide’ and ‘bird’ to search the following data- bases to query literature on rodenticide effects on non-raptor birds: US A Spearman's correlation was run to assess the relationship between Geological Survey's Digital Desktop Library (http://internal.usgs.gov/ the number of incidents documented and the number of species report- library/), United States Department of Agriculture's AGRICultural OnLine ed in the incidents from 15 countries (http://www.socscistatistics.com/ Access (http://agricola.nal.usda.gov/), GreenFILE (greeninfoonline.com), tests/spearman/default2.aspx). Two-tailed, two sample z tests for pro- ScienceDirect (http://www.sciencedirect.com/), IngeniaConnect (http:// portions (http://www.socscistatistics.com/tests/ztest/Default2.aspx) www.ingentaconnect.com/), Journal Storage (JSTOR, http://www.jstor. were performed to compare the number of species and the number of org/), BioOne (http://www.bioone.org/), Scopus (https://www.scopus. incidents reported with respect to the surveillance method and the pur- com/), Web of Science (http://apps.webofknowledge.com/), Google pose of the application. Scholar (https://scholar.google.com/), United Kingdom Wildlife Incident Investigation Scheme reports. 3. Results and discussion (http://www.hse.gov.uk/pesticides/topics/reducing- environmental-impact/wildlife/wiis-quarterly-reports.htm; http:// 3.1. Overview www.hse.gov.uk/pesticides/topics/reducing-environmental-impact/ wildlife/annual-report-pesticide-poisoning-of-animals.htm; https:// My query showed that non-raptor birds consumed rodenticide-con- www.sasa.gov.uk/animal-poisoning-reports), and the US EPA Incident taining baits, placebo baits, and rodenticide contaminated prey. I found Data System records (https://www.epa.gov/pesticide-science-and- 641 rodenticide incidents involving 17 Orders, 58 Families, and at least assessing-pesticide-risks/guidance-using-incident-data-evaluating- 190 non-raptor bird species (taxa of some birds were not specified to listed-and). A written request to the US EPA is required to acquire copies genus and species, ex. duck, Appendix 1). The magnitude of the inci- of individual incidents from its Incident Data System (R. Miller, US EPA, dents ranged from a single bird (e.g. Stone et al., 1999)topopulationde- pers. comm.). clines in areas treated with rodenticides (e.g. Apa et al., 1991; Howald et I reviewed all incident records retrieved by my query and discarded al., 1999, 2009; McClelland, 2002; Powlesland et al., 2000; Taylor, 1984). incidents from laboratory experiments (e.g. acute toxicity values in Nineteen anticoagulant and non-anticoagulant rodenticide active ingre- Godfrey, 1985; Spurr, 1993), duplications of incidents (e.g. an incident dients were associated with the incidents (Fig. 1). These rodenticides involving Australasian Swamphen (Porphyrio melanotus) is cited as are broad-spectrum vertebrate control agents that pose a significant Veitch, 2002a in Appendix 1, although the incident was also reported risk to all bird species. as personal communication in Eason and Spurr, 1995), and unpublished In 532 incidents, 168 species exhibited overt adverse effects. My tally incidents with the exception of records from the US EPA Incident Data for adverse effects included birds that were confirmed to have died from System. Therefore, the incidents listed in Appendix 1 represent unique rodenticides (e.g. Vyas et al., 2013), birds that were adequately pre- records for free-ranging wild and domesticated non-raptor birds. Fur- sumed by the author to have died from rodenticide exposure (e.g. thermore, incidents in non-raptor zoo birds were also included in Ap- Empson and Miskelly, 1999; McClelland, 2002, also see Section 3.5) pendix 1 because although these birds were not completely free- and moribund birds. The latter group included birds that ultimately ranging, they did consume rodenticides of their own volition, thus sug- died (e.g. Blus et al., 1985) and birds that survived because of medical gesting that wild conspecifics may also be at risk from rodenticides. The treatment (e.g. James et al., 1998; Swenson and Bradley, 2013). My incident records presented in Appendix 1 range in dates from 1931 to query also returned 94 rodenticide incidents involving 41 species (18 2016. of these species were in addition to the 168 tallied above) where only Based on the information provided in the incident records, I catego- the evidence of rodenticide exposure could be confirmed (Appendix rized each record, when possible, by the surveillance method (active or 1). These incidents documented non-raptor bird exposures to rodenti- passive) that initially detected the incident and by the purpose of the cides but did not provide evidence of an adverse effect. Incident reports application (human welfare or ecological restoration). I considered an deemed as exposure included observations of birds feeding on the ro- incident to have been documented using passive surveillance if it was, denticide bait (e.g. Veitch, 2002b) or poisoned prey (e.g. James et al., at least initially, voluntarily reported to the authorities (ex. public's ser- 1990); beak marks on rodenticide stations and blocks (e.g. Taylor and endipitous encounters with poisoned birds) and I identified an incident Thomas, 1993); rodenticide-colored droppings (Vyas et al., 2013); pres- to be from active surveillance if the initial documentation of the incident ence of tracer dye in droppings (e.g. Fellows et al., 1988); rodenticide was collected through field work with the objective of documenting ad- residues in live, overtly healthy birds (e.g. Spurr et al., 2015); and roden- verse effects on birds. I defined field work as planned searches for inci- ticide residues in dead birds that were below the threshold levels ex- dents following operational (e.g. van Klink and Crowell, 2015)or pected to cause an adverse effect (e.g. Pitt et al., 2015). Rodenticide experimental rodenticide applications (e.g. Ramey and Sterner, 1995) residues were measured in the last two categories but were not report- and systematic interviews with applicators and landowners about wild- ed for all incidents. For example, WIIS only reported the active ingredi- life mortalities they may have observed (e.g. Linsdale, 1931). ent and whether the detected rodenticides could be considered to be 70 N.B. Vyas / Science of the Total Environment 609 (2017) 68–76

Fig. 1. Rodenticides involved in non-raptor bird incidents. the cause of the incident. For incidents where rodenticide residues were during the season when the birds are not breeding and many of the measured, the small rodenticide concentrations or the lack of residues, bird species have migrated away in order to minimize non-target expo- in some cases, may be artifacts of rodenticide excretion and degradation sures (DSEWPaC, 2010). However, some resident species, opportunistic that could have occurred between lethal exposure and mortality foragers, and even migrants that are either late in departing or arrive (Record and Marsh, 1988) and between the mortality and when the car- while the bait is still potent from an earlier application, may be killed cass was collected for analysis (Brown et al., 2007; Eason et al., 2013). (Dowding et al., 1999; DSEWPaC, 2010; Howald et al., 2009; Salmon et Sublethal rodenticide exposures may also contribute to the small resi- al., 2010). The timing of rodenticide applications for human welfare (i.e. due concentrations. Sublethal rodenticide exposures have not yet agriculture, public health), however, is not dictated by bird biology, and been linked to direct or indirect adverse effects for non-raptor birds resident and migratory birds can be exposed and poisoned (e.g. Koenig but studies on sublethal rodenticide exposures on mammals and suble- and Reynolds, 1987; Vyas et al., 2013). thal pesticide exposures on birds have shown that low level pesticide Rodenticide chemistry dictates its toxicity, mode of action, pharma- exposures can increase an animal's susceptibility to various stressors cokinetics (absorption, distribution, metabolism, excretion) and its time (e.g. Galindo et al. 1985; Vyas et al., 2017; Zeakes et al., 1981). Therefore, course of toxic events (e.g. in Eason et al., 2002;inRecord and Marsh, necropsy of a carcass may suggest a distal cause of death (e.g. starva- n1988;i Savarie, 1981). Once a rodenticide is released into the environ- tion), whereas the ultimate cause of the mortality may be rodenticide ment, its chemistry and formulation interact with abiotic factors (e.g. exposure. For example, based on post-mortem examinations, the cause weather and soil and water chemistry) to affect the rodenticide's distri- of death of a heron (spp.) and a European Badger (Meles meles)found bution and persistence in the environment (Apa et al., 1991; Booth et al., in a woodland was determined to be starvation although bromadiolone 1999; Eason et al., 2000, 2011, 2013; Masuda et al., 2014; McClelland, and difenacoum residues were confirmed in their livers (WIIS, 2012). 2002; Merton et al., 2002; Spurr et al., 2005; US EPA, 1998; van Klink Similarly, starvation was attributed as the cause of death for Little Pen- and Crowell, 2015). Non-raptor bird incidents have been evoked by var- guins (Eudyptula minor) with sublethal brodifacoum residues (Fisher et ious rodenticide formulations including blocks (Howald et al., 1999), ce- al., 2011). The analytical detection limits for the incidents categorized as real based pellets (in Spurr and Powlesland, 1997; Swenson and exposure in Appendix 1 ranged 0.001 μg/g to 0.5 μg/g. Bradley, 2013), pastes and jams (Pryde et al., 2013; Spurr, 2000), liquids Fifteen placebo rodenticide incidents involving 13 species were (McIlroy, 1983), powders (https://www.aphis.usda.gov/publications/ found and four of these species were in addition to the 168 species wildlife_damage/content/printable_version/fs_m44_device.pdf), carrot above. Twenty-six incident records involving 21 non-raptor bird species baits (in Morriss et al., 2016; Powlesland et al., 1999) and loose grain in zoos were found (Table 2). Zoos rely on rodenticides to control verte- baits (Proulx, 2011; Vyas et al., 2013). Non-raptor bird incidents have brate pests and although care is taken to protect captive birds from ac- occurred following rodenticide applications above ground (Brown, cidental exposure, birds have been poisoned from feeding on bait 1997; Hegdal et al., 1986; Sánchez-Barbudo et al., 2012), below ground scattered in the exhibits by rodents (Swenson and Bradley, 2013) and (Apa et al., 1991; Vyas et al., 2013), in bait stations (Pryde et al., 2013; from feeding on rodenticide contaminated prey (in Borst and Taylor, 1984), and in meat (McIlroy, 1983). Counotte, 2002; Hernandez-Moreno et al., 2013). Biotic factors that influence rodenticide exposure and poisoning of non-raptor birds include the species present and their diet, foraging be- 3.2. Factors that contribute to non-raptor bird exposure and poisoning havior, and morphology. Granivorous, invertivorous, carnivorous, and omnivorous non-raptor bird species that typically or opportunistically The diversity of the non-raptor bird species exposed to and poisoned feed on the ground; are inquisitive and readily accept novel foods by rodenticides is a reflection of the complex interactions among the an- (Spurr, 1993; Eason and Spurr, 1995; Howald et al., 1999; Robertson thropogenic, abiotic, and biotic components of the ecosystem. In addition et al., 1999; van Klink and Crowell, 2015); are habituated to humans to developing and manufacturing rodenticide products, humans govern (Empson and Miskelly, 1999); forage over large areas (DSEWPaC, the spatiotemporal availability of rodenticides to birds through pesticide 2010; Koenig and Reynolds, 1987); feed on the target pest (DSEWPaC, regulations, education, enforcement (Eason et al., 2015; Statham, 2005; 2010; Eason and Spurr, 1995); and/or exploit ephemeral food resources https://www.epa.gov/endangered-species/anticoagulant-prairie-dog- (Dowding et al., 1999; DSEWPaC, 2010) appear to be at greater risk of bait-risk-mitigation-measures-protect-endangered), and compliance rodenticide exposure and poisoning than other non-raptor bird species with the rodenticide label (Olea et al., 2009; Proulx, 2014; Statham, (Eason and Spurr, 1995; Ebbert and Burek-Huntington, 2010; van Klink 2005; Tosh et al., 2011; Vyas, 2013). The purpose of the application can and Crowell, 2015). Although non-raptor bird species are more likely to influence its timing and this in turn can affect non-raptor bird exposure. feed on rodenticide bait when other food items are scarce (Howald et Often rodenticide applications for ecological restoration are conducted al., 1999; Poppenga et al., 2005; Vyas et al., 2013), it is noteworthy N.B. Vyas / Science of the Total Environment 609 (2017) 68–76 71 that even well fed birds in zoos have been poisoned (Appendix 1). These Table 1 incidents suggest that for some wild individuals and species, the risks of Numbers of rodenticide incidents and non-raptor bird species by country. rodenticide exposure due to their inquisitive nature and/or familiarity Country Incidents Species to humans may outweigh the protection afforded by sufficient food Australia 36 27 availability. Primary exposure through the consumption of rodenticide Canada 18 14 baits can result in mortality from the toxicity of the rodenticide's active Czechoslovakia 1 1 ingredient and through gizzard impaction by paraffin, an inert ingredi- France 5 5 ent used in some block and pellet formulations to improve weatherabil- Germany 5 3 Israel 5 5 ity (Blus et al., 1985). Secondary rodenticide exposure and poisoning of Japan 1 1 non-raptor birds has occurred through consumption of contaminated Mongolia 5 5 invertebrate and vertebrate prey. Some examples of rodenticide expo- New Zealand 138 51 sure and poisoning via invertebrates include potential exposure of Seychelles 9 9 Spain 15 12 Song Sparrows (Melospiza melodia) through carrion insects on Thailand 2 2 brodifacoum poisoned Norway Rat (Rattus norvegicus) carcasses The Netherlands 6 3 (Howald et al., 1999); mortalities of Red-breasted Dotterels (Charadrius United Kingdom 102 21 obscurus) that fed on Sandhoppers (Talorchestia spp.) that had con- United States 293 86 sumed brodifacoum pellets (Dowding et al., 2006); mortalities of New Zealand Robin (Petroica australis) nestlings fed brodifacoum contaminated invertebrates (Masuda et al., 2014); mortalities of captive Gray- 2013). Incident detection through passive surveillance, however, is hin- cowled Wood-rail (Aramides cajanea) and Black Grouse (Tetrao tetrix) dered by the inherent challenges of observing, reporting, and fi after feeding on snails that had consumed brodifacoum and difenacoum con rming the event. At the landscape level, it is not possible to search bait (Hernandez-Moreno et al., 2013); and poisonings of several non- the vast areas subjected to rodenticide applications. On a local scale, the raptor bird species in zoos via ants and cockroaches contaminated by interactions among anthropogenic, biological, and abiotic factors often fl fi brodifacoum (in Erickson and Urban, 2004). Examples of rodenticide in uence the detection, reporting, and con rmation of a rodenticide in- exposure and poisoning of non-raptor bird species through contaminat- cident. Additionally, citizen apathy and the lack of knowledge that the ed vertebrate prey include observations of corvids (Corvus spp.) and a incident should be reported and to whom it should be reported can fi California Gull (Larus californicus) feeding on strychnine-killed hamper the noti cation of the incident to the authorities (Ward et al., Richardson's Ground squirrels (Urocitellus richardsonii)(James et al., 2006; Vyas, 1999). Active surveillance can also generate biased incident 1990); mortalities of Common Ravens (Corvus corax)thatfedon information due to limited funding for conducting the surveillance; brodifacoum-poisoned rats (Howald et al., 1999); and mortalities of level of training of the human searchers; method, intensity, timing, seabirds that scavenged on brodifacoum-poisoned European Rabbits and frequency of the surveillance; and a focus on only selected species (Oryctolagus cuniculus)(DSEWPaC, 2010). (Borges et al., 2014; Ford, 2006; Linz et al., 1991; Smallwood, 2007). Bird morphology can facilitate access to rodenticides. Small birds can Biological factors such as the habitat, scavenger population, and spe- enter bait station boxes (Elliott et al., 2014; Taylor and Thomas, 1993) cies' behavior and morphology can affect incident detection by humans and burrow entrances (Vyas et al., 2013) to feed on the rodenticide (Vyas, 1999). Severe adverse effects (e.g. moribundity and mortality) bait and invertebrate prey that are attracted to the rodenticide bait are the most likely incidents to be recognized by humans whereas sub- (Craddock, 2003; Dunlevy et al., 2000; Spurr and Drew, 1999). Strong tle sublethal impairments (e.g. physiological or behavioral disruption billed birds can break into bait station boxes to feed on rodenticide that may harm the health and long-term survival of a bird), especially bait (Howald et al., 1999; Taylor and Thomas, 1993). Birds with long when birds do not exhibit overt signs of rodenticide exposure, are likely necks can reach the rodenticide in some tube bait stations to be missed by humans. Therefore sublethal adverse effects of rodenti- fi (Shivaprasad and Galey, 2001; Taylor, 1984) whereas birds with short cides on non-raptor bird species are rarely documented from the eld bills that feed on the ground are more likely to be exposed after surface (Hoare and Hare, 2006; Howell and Wishart, 1969). fl application of rodenticides (Robertson et al., 1999). However, birds that Abiotic factors (e.g. weather) in uence the rate of carcass decompo- probe the ground may also encounter rodenticides that have been ap- sition and rodenticide degradation (Eason et al., 2013; Fisher et al., plied into artificial tunnels to control fossorial rodents (Giraudoux et 2011; Masuda et al., 2014; Morriss et al., 2016; Towns et al., 1993) al., 2006; Hegdal and Gatz, 1976; Pierce and Montgomery, 1992). and therefore can limit the time during which chemical analysis can be conducted to confirm a rodenticide as the cause of the adverse effect. 3.3. Factors that contribute to documenting incidents A rodenticide's half-life in a bird, bioaccumulation potential, time- course of action, vague or inconsistent clinical signs, interactions with Despite rodenticide use worldwide, my query retrieved non-raptor other stressors (e.g. starvation), absence of the toxicant in the gastroin- bird incidents from only 15 countries and records from the United testinal tract, and the absence of residues in tissue at time of analysis can fi States, New Zealand, and The United Kingdom comprised ~83% of the also confound the con rmation of a rodenticide as the cause of an ad- incidents (Table 1). For the 15 countries, there was a strong positive cor- verse effect (Bildfell et al., 2013; Dowding et al., 1999; Fisher et al., relation between the number of incidents documented and the diversity 2011; Masuda et al., 2014; Morgan et al., 1996; Poppenga et al., 2005; Powlesland et al., 2000; Sánchez-Barbudo et al., 2012; Sarabia et al., of affected species (rs = 0.964, p b 0.001; Table 1). When considering the results of the correlation analysis with the fact that few or no non- 2008). Consequently, the known incident records represent only a frac- raptor bird incidents have been reported from the majority of the coun- tion of the incidents that have occurred (Balcomb, 1986; Kostecke et al., tries in the world that use rodenticides, it is reasonable to suggest that 2001; Peterson et al., 2001). Nevertheless, the incident records do pro- there is a need for increasing the awareness of the hazards of rodenti- vide invaluable insights into the hazards of rodenticides following oper- cides to non-raptor birds and for establishing or improving infrastruc- ational applications (Vyas, 1999). ture to document the incidents and to make the data publically accessible. However, socio-economic conditions in some countries 3.4. Influence of surveillance method and purpose of application on incident may prevent monitoring for non-raptor birds incidents. reporting Documentation of incidents from the field is dependent on detecting and reporting the incident and confirming the cause of death by residue To improve the understanding of the factors that affect the likeli- analysis, necropsy, and histopathology (Bildfell et al., 2013; Vyas et al., hood of detecting non-raptor bird incidents, I analyzed the incidents 72 N.B. Vyas / Science of the Total Environment 609 (2017) 68–76 by the surveillance method used to detect the incidents. My query net- methods following rodenticide applications for human welfare (77 vs. ted 128 species from 267 rodenticide incidents when active surveillance 334 incidents), a significantly greater number of species were detected was employed and 63 species from 334 rodenticide incidents from pas- in proportion to the number of incidents found through active surveil- sive surveillance. The surveillance method was not specified for 14 ro- lance than through passive surveillance (z = 7.32, p b 0.01). denticide incidents involving 12 species. Significantly greater number of species were detected in proportion to the number of incidents 3.5. Uncertainties associated with the analyses found through active surveillance than with passive surveillance (z = 7.61, p b 0.01). The greater number of rodenticide incidents found The vertebrate control agents and bird taxa presented here should with passive surveillance than with active surveillance may be a func- not be considered a comprehensive review of the hazards of rodenti- tion of passive surveillance being used more commonly than active sur- cides to non-raptor birds. Uncertainties associated with my analysis oc- veillance because the latter is considerably more resource intensive curred at three levels: incident collection and confirmation, incident (Ritz et al., 2005; Vogt et al., 1983). I suggest, however, that the greater report accessibility, and incident record interpretation. The first two un- number of species detected by active surveillance than with passive sur- certainties determined the number of incidents that were included in veillance is a reflection of the surveillance method. Passive surveillance my analysis. Uncertainties associated with incident collection and con- generally relies on serendipitous discoveries of incidents and the will- firmation, in addition to the anthropogenic, abiotic, and biological fac- ingness of the public to report the incidents to the appropriate authori- tors discussed in Section 3.3, are depended on the presence of an ties whereas for active surveillance, the detection and documentation of infrastructure that supports surveillance for non-raptor bird incidents adverse effects to non-target species is of central interest. The focused and determination of their causality. A lack of a systematic incident approach of active surveillance resulted in the greater number of species monitoring infrastructure for birds is expected for poor and developing detected in proportion to the number of incidents found. countries. However, some developed countries with an effective roden- The species-incident proportions for the two surveillance methods ticide monitoring infrastructure have not reported non-raptor rodenti- may be biased by the purpose of the application (ecological restoration cide incidents. The paucity of non-raptor incident reports from these or human welfare). I determined 71% (425) of all incident records (not countries may result from a bias towards raptors. For example, including zoos and records with undetermined purpose of application) Gómez-Ramírez et al. (2014) found 52 contaminant monitoring to be due to rodenticide applications for human welfare whereas only schemes with raptors across 44 European countries and schemes from 29% (177) of the incidents were from applications for ecological restora- six of the countries have included rodenticides. Of these, only one tion (Table 2). All records for ecological restoration involved rodenticide scheme (Wildlife Incident Investigation Scheme from the United King- use on islands to protect native wildlife and therefore active surveil- dom) systematically catalogs rodenticide incidents for raptor and non- lance was employed to detect non-target incidents following rodenti- raptor birds. I suggest that the preference for monitoring raptors over cide applications. Rodenticide applications for human welfare, non-raptor birds may at least be partially driven by 1) the traditional however, were conducted to protect human enterprises (e.g. agricultur- view of a simple exposure pathway where rodents eat rodenticides rap- al yield, human health) and therefore detection of adverse effects to tors feed on the contaminated rodents (Gómez-Ramírez et al., 2014; non-target birds was not a priority (Linsdale, 1931). Thus, following ro- Ruiz-Suárez et al., 2014) and 2) the consideration that raptors are denticide use for human welfare, only 77 incidents were detected using often used as biomonitors of environmental health because raptors active surveillance whereas 334 incidents were detected using passive are top-level predators. However, predatory (invertivorous, omnivo- surveillance (Table 2). Because active and passive surveillance methods rous, and carnivorous) non-raptor species can also be exposed to antico- were employed after applications for human welfare but only active agulant rodenticides through contaminated prey (e.g. Howald et al., surveillance followed ecological restoration applications, I compared 1999; Dowding et al., 2006; Hernandez-Moreno et al., 2013; Masuda the species and incident numbers for the two surveillance methods fol- et al., 2014) and therefore can also serve as biomonitors of environmen- lowing only human welfare applications. Despite the large difference tal health. between the number of incidents detected by the two surveillance Uncertainties associated with incident report accessibility are two- fold. First, despite my searches for incident records from several sources (see Section 2.1) and encompassing 86 years (1931–2016), it is reason- Table 2 able to conclude that I missed some records that could be available to Summary of rodenticide incidents and non-raptor bird species included in Appendix 1. me. Second, not all incident records are publically available. The latter Incidents Species case is influenced by the presence of an infrastructure that promotes Total 641 190 dissemination of the incident records. For example, in my analyses, the greatest numbers of incidents were reported from the United States, Type of effect New Zealand, and the United Kingdom, respectively. The large number Mortality 532 168 Exposure 94 41 of incidents from the United States is attributed not only to the publical- Placebo 15 13 ly available journal publications but also to my access to the publically unavailable US EPA's Incident Data System. Records from this database Purpose for the application Human welfare 425 99 comprised 58% of the United States reports. The large number of non- Ecological restoration 177 92 raptor bird incidents from the United Kingdom is due to the publically accessible Wildlife Incident Information System. Journal publications Surveillance method Active 267 128 documenting non-raptor bird incidents from New Zealand's invasive Passive 334 63 mammal eradication program resulted in the third largest number of incident compilations; although I found no bird incidents that may have Purpose and surveillance Human welfare and active 77 46 occurred following rodenticide applications conducted exclusively for Human welfare and passive 334 63 human welfare in New Zealand. The dearth of records from the coun- Ecological restoration and active 177 92 tries listed in Table 1 and countries not included in the table does not Ecological restoration and passive 0 0 imply that no incidents have occurred but suggests a lack of or a limited Active surveillance but Purpose not determined 13 5 infrastructure for collecting, confirming and publishing the rodenticide Human welfare but Surveillance method not determined 14 12 incidents of non-raptor birds in a publically accessible outlet. For exam- Zoo ple, despite infrastructural capabilities for documenting anticoagulant Zoo 26 21 rodenticide human incidents, Denmark, Norway, and Sweden have N.B. Vyas / Science of the Total Environment 609 (2017) 68–76 73 only recently published on rodenticide exposure and poisoning of birds First, the information may convince some rodenticide applicators to (albeit on raptors) in journals (Christensen et al., 2012; Langford et al., place greater emphasis on ensuring rodenticide label compliance with 2013; Laakso et al., 2010; Nordström et al., 2013). regards to application and mitigation. Second, public enlightenment of In my analysis, the uncertainties associated with interpretation of in- the hazards may increase the likelihood of reporting the incidents. cident records were driven by the quality of the information provided in Third, non-raptor birds may now be included in monitoring schemes. the records. Incident record quality ranged from results that verified the Fourth, non-raptor bird incidents can clarify potential routes of rodenti- rodenticide exposure and adverse effects through necropsy, histopa- cide exposures to their bird predators, raptors (Elliott et al., 2016). Last- thology, and/or residue analysis (e.g. Bildfell et al., 2013; Vyas et al., ly, an improvement in the quantity and quality of incident reports may 2013) to reporting only that unidentified gamebirds had died after feed- strengthen the predictions of harm characterized by risk assessments. ing on a rodenticide at bait stations (e.g. Key, 1990). The latter incident Supplementary data to this article can be found online at http://dx. and similar records were excluded from my analysis. Within the spec- doi.org/10.1016/j.scitotenv.2017.07.004. trum of usable records, some incident reports did not confirm the cause of death because carcasses had decomposed (e.g. Fisher et al., Acknowledgements 2011), had been scavenged (e.g. Brown, 1997), carcasses were found but discarded (e.g. Veitch, 2002a), live birds banded before the rodenti- I thank W.N. Beyer and M. Panger, and B.A. Rattner for their thought- cide application were not sighted after application (e.g. Empson and ful review of the manuscript. I also express gratitude to M. Panger for Miskelly, 1999), or no necropsy or residue analysis were conducted approving access to the US EPA Incident Database System and R. Miller even when fresh carcasses were recovered (e.g. in Dolgormaa, 2004). for his assistance with installing the US EPA Incident Database System For incident records without verified cause of death, I relied on the on my computer. I thank L. Garrett and S. Beliew for retrieving articles author's and my judgements to determine if these incidents would be and T. Mabee for the inspiration for preparing this document. I am in- included in my analysis. Four examples follow: When birds that were debted to the anonymous journal reviewers for their suggestions for im- banded before rodenticide application could not be located after the approving the manuscript. This work was conducted as part of my work plication, I relied on the authors' assessments for the possible cause of duties and was supported by the USGS Patuxent Wildlife Research Cen- the disappearances (Empson and Miskelly, 1999; McClelland, 2002). ter. Any use of trade, product, or firm names is for descriptive purposes Veitch (2002a) reported carcasses of 11 bird species that were found only and does not imply endorsement by the U.S. Government. after a brodifacoum application, but based on necropsy or residue analysis, I included only six of the species in my analysis. Nevertheless it is References possible that at least some of the birds of the remaining five species could have died from brodifacoum because these species have been poi- Apa, A.D., Uresk, D.W., Linder, R.L., 1991. Impacts of black-tailed prairie dog rodenticides on nontarget passerines. Great Basin Naturalist 51:301–309. http://www.fs.fed.us/ soned after similar applications elsewhere (Appendix 1). By contrast, I rm/pubs_journals/1991/rmrs_1991_uresk_d001.pdf (Available, accessed November accepted incident records with suspected bromadiolone poisoning of 11, 2016). 3 Ruddy Shelducks, 3 Whooper Swans, 149 Demoiselle Cranes, 152 Her- Balcomb, R., 1986. Songbird carcasses disappear rapidly from agricultural fields, Auk. 103:pp. 817–820. https://doi.org/10.1648/0273-8570-72.1.150 (Available, accessed ring Gulls, and 20 Daurian Jackdaws in Mongolia based on March 16, 2017). bromadiolone's history of bird kills (Appendix 1), the incident's diversi- Berny, P.J., Buronfosse, T., Buronfosse, F., Lamarque, F., Lorgue, G., 1997. Field evidence of ty and magnitude, and the use of aerial application over a large area (in secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo)by bromadiolone, a 4-year survey. Chemosphere 35, 1817–1829. Dolgormaa, 2004). Similarly, although only one of 11 thallium incidents Bildfell, R.J., Rumbeiha, W.K., Schuler, K.L., Meteyer, C.U., Wolff, P.L., Gillin, C.M., 2013. A reported by Linsdale (1931) was analytically confirmed, I considered review of episodes of zinc phosphide toxicosis in wild geese (Branta spp.) in Oregon thallium to be the cause of the remaining 10 incidents compiled by (2004–2011). J. Vet. Diagn. Investig. 25:162–167. http://dx.doi.org/10.1177/ fi 1040638712472499 (Available, accessed November 11, 2016). Linsdale. My con dence that thallium was responsible for the 10 inci- Blus, L.J., Henny, C.J., Grove, R.A., 1985. Effects of pelletized anticoagulant rodenticides on dents was derived from thallium's toxicity, the fact that it was wide- California quail. J. Wildl. Dis. 21:391–395. http://dx.doi.org/10.7589/0090-3558-21.4. spread and commonly used for ground-squirrel control in California, 391 (http://www.bioone.org/doi/pdf/10.7589/0090-3558-21.4.391. Available, and Linsdale's meticulous vetting of incident data. accessed November 11, 2016). Booth, L.H., Ogilvie, S.C., Eason, C.T., 1999. Persistence of sodium monofluoroacetate (1080), pindone, cholecalciferol, and brodifacoum in possum baits under simulated 4. Conclusions rainfall. N. Z. J. Agric. Res. 42:107–112. http://dx.doi.org/10.1080/00288233.1999. 9513359 (Available, accessed November 11, 2016). Borges, S.L., Vyas, N.B., Christman, M.C., 2014. The influence of study species selection on Rodenticides with a variety of modes of action, formulations, and ap- estimates of pesticide exposure in free-ranging birds. Environ. Manag. 53, 416–428. plications methods have adversely affected a broad diversity of non- Borst, G.H.A., Counotte, G.H.M., 2002. Shortfalls using second-generation anticoagulant raptor bird taxa. In light of the above uncertainties, it is reasonable to rodenticides. J. Zoo Wildl. Med. 33, 85. Brown, K.P., 1997. Impact of brodifacoum poisoning operations on South Island robins suggest that the 641 incident records reported in Appendix 1, neverthe- Petroica australis australis in a New Zealand Nothofagus forest. Bird Conserv. Int. 7, less, underestimate the hazards of rodenticides to non-raptor birds. The 399–407. paucity of incident information on non-raptor birds does not necessarily Brown, L.E., Fisher, P., Wright, G., Booth, L., 2007. Measuring degradation of zinc phosphide residues in possum stomach contents. Bull. Environ. Contam. Toxicol. 79: imply a lack of hazard but may signify a lack of surveillance (Howald et 459–461. https://www.researchgate.net/profile/Penny_Fisher/publication/5968994_ al., 2009; Koenig and Reynolds, 1987; Proulx, 2011; Spurr and Measuring_degradation_of_zinc_phosphide_residues_in_possum_stomach_ Powlesland, 1997; Vyas, 2013) or an insensitive surveillance design contents/links/548a0c2f0cf214269f1ac175.pdf (Available, accessed June 07, 2017). Christensen, T.K., Lassen, P., Elmeros, M., 2012. High exposure rates of anticoagulant ro- (Veltman and Westbrooke, 2011). Several anthropogenic, abiotic, and denticides in predatory bird species in intensively managed landscapes in Denmark. biotic factors (Section 3.3 above) have been studied to explain the biases Arch. Environ. Contam. Toxicol. 63, 437–444. in incident detection, reporting, and confirmation. Here I analyzed an Craddock, P., 2003. Aspects of the ecology of forest invertebrates and the use of additional variable (surveillance method) that can also distort the quan- brodifacoum. Doctoral Dissertation. University of Auckland, New Zealand :p. 206. https://researchspace.auckland.ac.nz/bitstream/handle/2292/316/02wholepart2. tity and quality of incident data. The species-incident proportions calcu- pdf?sequence=10 (Available, accessed November 11, 2016). lated here support that increasing active surveillance can improve our Dolgormaa, L., 2004. Toxic Issues in Mongolia. World Wildlife Fund:p. 6. http://assets. knowledge of the diversity of the affected non-raptor bird species panda.org/downloads/toxics_issues_in_mn__march04.pdf (Available, accessed Feb- ruary 28, 2017). whereas the less-resource intensive passive surveillance can be used Dowding, J.E., Murphy, E.C., Veitch, C.R., 1999. Brodifacoum residues in target and non- to document a greater number of incidents. target species following an aerial poisoning operation on Motuihe Island, Hauraki Incident data provide insight into the hazards of rodenticides follow- Gulf, New Zealand. N. Z. J. Ecol. 23:207–214. http://newzealandecology.org/nzje/ 2076.pdf (Available, accessed November 11, 2016). ing operational applications. Knowledge that rodenticides are hazard- Dowding, J.E., Lovegrove, T.G., Ritchie, J., Kast, S.N., Puckett, M., 2006. Mortality of north- ous to non-raptor birds can benefit their conservation in several ways. ern New Zealand dotterels (Charadrius obscurus aquilonius) following an aerial 74 N.B. Vyas / Science of the Total Environment 609 (2017) 68–76

poisoning operation. Notornis 53:235–239. http://notornis.osnz.org.nz/system/files/ fd88-11e6-b084-00000aacb361&acdnat=1488267678_ Notornis_53_2_235.pdf (Available, accessed November 11, 2016). f63fd031436433d7bdf08dac49cbe09d (Available, accessed February 28, 2017). DSEWPaC, 2010. Department of Sustainability, Environment, Water, Population and Com- Hegdal, P.L., Gatz, T.A., 1976. Hazards to wildlife associated with underground strychnine munities and Tasmanian Department of Primary Industries, Parks, Water and Envi- baiting for pocket gophers. Proceedings of the 7th Vertebrate Pest Conference (1976) ronment 2010: Macquarie Island Pest Eradication Program - Review of the Impact :pp. 258–266. http://digitalcommons.unl.edu/cgi/viewcontent.cgi?article= of 2010 Aerial Baiting on Non-target Species - Final Report, Canberra, Australia. : 1023&context=vpc7 (Available, accessed November 11, 2016). p. 17. http://www.parks.tas.gov.au/file.aspx?id=20985 (Available, accessed June 1, Hegdal, P.L., Fagerstone, K.A., Gatz, T.A., Glahn, J.F., Matschke, G.H., 1986. Hazards to wild- 2017). life associated with 1080 baiting for California ground squirrels. Wildl. Soc. Bull. 14: Dunlevy, P.A., Campbell, E.W., Lindsey, G.D., 2000. Broadcast application of a placebo ro- 11–21. http://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=2435&context= denticide bait in a native Hawaiian forest. Int. Biodeterior. Biodegrad. 45:199–208. icwdm_usdanwrc (Available, accessed November 11, 2016). http://removeratsrestorehawaii.org/wp-content/uploads/2010/03/Dunlevy-et-al- Hernandez-Moreno, D., de la Casa-Resino, I., Lopez-Beceiro, A., Fidalgo, L.E., Soler, F., 2000.pdf (Available, accessed November 11, 2016). Perez-Lopez, M., 2013. Secondary poisoning of non-target animals in an Ornitholog- Eason, C.T., Spurr, E.B., 1995. Review of the toxicity and impacts of brodifacoum on non- ical Zoo in Galicia (NW Spain) with anticoagulant rodenticides: a case report. Vet. target wildlife in New Zealand. N. Z. J. Ecol. 22:371–379. http://dx.doi.org/10.1080/ Med. 58:553–559. http://dx.doi.org/10.1016/j.scitotenv.2012.01.028. http://www. 03014223.1995.9518055. http://www.tandfonline.com/doi/pdf/10.1080/03014223. agriculturejournals.cz/publicFiles/106223.pdf (Available, accessed November 11, 1995.9518055?needAccess=true (Available, accessed November 11, 2016). 2016). Eason, C.T., Wickstrom, M., Henderson, R., Milne, L., Arthur, D., 2000. Non-target and sec- Hoare, J.M., Hare, K.M., 2006. The impact of brodifacoum on non-target wildlife: gaps in ondary poisoning risks associated with cholecalciferol. N. Z. Plant Protect. 53: knowledge. N. Z. J. Ecol. 30:157–167. https://www.researchgate.net/profile/Kelly_ 299–304. https://nzpps.org/journal/53/nzpp_532990.pdf (Available, accessed No- Hare/publication/242079627_The_impact_of_brodifacoum_on_non-target_wildlife_ vember 11, 2016). gaps_in_knowledge/links/0c960528ea19ae2912000000.Pdf (Available, accessed No- Eason, C.T., Murphy, E.C., Wright, G.R., Spurr, E.B., 2002. Assessment of risks of brodifacoum vember 11, 2016). to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48. https:// Howald, G.R., Mineau, P., Elliott, J.E., Cheng, K.M., 1999. Brodifacoum poisoning of avian www.researchgate.net/profile/Eric_Spurr/publication/263597953_Assessment_of_ scavengers during rat control on a seabird colony. Ecotoxicology 8:431–447. http:// Risks_of_Brodifacoum_to_Non-target_Birds_and_Mammals_in_New_Zealand/links/ s3.amazonaws.com/academia.edu.documents/40202191/Brodifacoum_Poisoning_ 53e802f10cf2fb748723f647.pdf (Available, accessed November 11, 2016). of_Avian_Scavenger20151120-29225-13kzk4t.pdf?AWSAccessKeyId= Eason, C., Miller, A., Ogilvie, S., Fairweather, A., 2011. An updated review of the toxicology AKIAJ56TQJRTWSMTNPEA&Expires=1479524280&Signature=Qrwe4pJkhwGT% and ecotoxicology of sodium fluoroacetate (1080) in relation to its use as a pest con- 2BM%2FvFLvnyNMWMbo%3D&response-content-disposition=inline%3B% trol tool in New Zealand. N. Z. J. Ecol. 35:1–20. http://researcharchive.lincoln.ac.nz/ 20filename%3DBrodifacoum_Poisoning_of_Avian_Scavenger.pdf (Available, accessed bitstream/handle/10182/4965/NZJEcol_1080.pdf?sequence=1 (Available, accessed November 11, 2016). November 11, 2016). Howald, G., Donlan, C.J., Faulkner, K.R., Ortega, S., Gellerman, H., Croll, D.A., Tershy, B.R., Eason, C., Ross, J., Blackie, H., Fairweather, A., 2013. Toxicology and ecotoxicology of zinc 2009. Eradication of black rats Rattus rattus from Anacapa Island. Oryx 44:30–40. phosphide as used for pest control in New Zealand. N. Z. J. Ecol. 37:1–11. https:// https://training.fws.gov/resources/course-resources/pesticides/IPM/Howald_etal_ researcharchive.lincoln.ac.nz/bitstream/handle/10182/7138/Eason%20et%20al.% 2010_Oryx.pdf (Available, accessed November 11, 2016). 20ZP%20NZES.pdf?sequence=1&isAllowed=y (Available, accessed June 07, 2017). Howell, J., Wishart, W.M., 1969. Strychnine poisoning in Canada geese. Bulletin of the Eason, C.T., Shapiro, L., Ogilvie, S., Clout, M., 2015. Trends in vertebrate pesticide use and Wildlife Disease Association. 5:p. 119. http://dx.doi.org/10.7589/0090-3558-5.2.119 the importance of a research pipeline for mammalian pest control in New Zealand, (Available, accessed November 11, 2016). Report No. 2754. :p. 60. http://www.cawthron.org.nz/media_new/publications/pdf/ James, P.C., Fox, G.A., Ethier, T.J., 1990. Is the operational use of strychnine to control 2016_05/CawRpt_2754.pdf (Available, accessed November 11, 2016). ground squirrels detrimental to burrowing owls? J. Raptor Res. 24, 120–123. Ebbert, S., Burek-Huntington, K., 2010. Anticoagulant residual concentration and poison- James, S.B., Raphael, B.L., Cook, R.A., 1998. Brodifacoum toxicity and treatment in a white- ing in birds following a large-scale aerial broadcast of 25-ppm brodifacoum bait for winged wood duck (Cairina scutulata). J. Zoo Wildl. Med. 29, 324–327. rat eradication on Rat Island, Alaska. In: Timm, R.M., Fagerstone, K.A. (Eds.), Proceed- Key, G.E., 1990. Control of the African striped ground squirrel, Xerus erythropus,inKenya. ings of the Vertebrate Pest Conference. 24, pp. 153–160. Proceedings of the Fourteenth Vertebrate Pest Conference 1990 :pp. 99–103. http:// Elliott, J.E., Hindmarch, S., Albert, C.A., Emery, J., Mineau, P., Maisonneuve, F., 2014. Expo- digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1047&context=vpc14 (Avail- sure pathways of anticoagulant rodenticides to nontarget wildlife. Environ. Monit. able, accessed March 02, 2017). Assess. 186, 895–906. van Klink, P., Crowell, M., 2015. Kea (Nestor notabilis) survivorship through a 1080 oper- Elliott, J.E., Rattner, B.A., Shore, R.F., van den Brink, N.W., 2016. Paying the pipers: mitigat- ation using cereal baits containing the bird repellent d-pulegone at Otira, central ing the impact of anticoagulant rodenticides on predators and scavengers. Bioscience Westland. DOC Research and Development Series. 344, p. 13 (http:// 66, 401–407 (//doi.org/10.1093/biosci/biw028. Available, accessed November 11, www.doc.govt.nz/documents/science-and-technical/drds344entire.pdf. Available, 2016). [accessed November 11, 2016]). Empson, R.A., Miskelly, C.M., 1999. The risks, costs and benefits of using brodifacoum to Koenig, W.D., Reynolds, M.D., 1987. Potential poisoning of yellow-billed magpies by com- eradicate rats from Kapiti Island, New Zealand. N. Z. J. Ecol. 23:241–254. http:// pound 1080. Wildl. Soc. Bull. 15, 274–276. newzealandecology.org/nzje/2081.pdf (Available, accessed November 11, 2016). Kostecke, R.M., Linz, G.M., Bleier, W.J., 2001. Survival of avian carcasses and photographic Erickson, W.A., Urban, D.J., 2004. Potential Risks of nine Rodenticides to Birds and Nontar- evidence of predators and scavengers. J. Field Ornithol. 72:439–447. http://dx.doi. get Mammals: A Comparative Approach. US Environmental Protection Agency, Office org/10.1648/0273-8570-72.3.439 (Available, accessed March 16, 2017). of Prevention, Pesticides and Toxic Substances, Washington, DC:p. 225. http:// Laakso, S., Suomalainen, K., Koivisto, S., 2010. Literature Review on Residues of Anticoag- pesticideresearch.com/site/docs/bulletins/EPAComparisonRodenticideRisks.pdf ulant Rodenticides in Non-Target Animals. Nordic Council of Ministers:p. 47. https:// (Available, accessed April 1, 2017). books.google.com/books?hl=en&lr=&id=SeEyqY8_4_UC&oi=fnd&pg=PA5&dq= Fellows, D.P., Pank, L.F., Engeman, R.M., 1988. Hazards to birds from zinc phosphide rat Literature+review+on+residues+of+anticoagulant+rodenticides+in+non- bait in a macadamia orchard. Wildl. Soc. Bull. 16, 411–416. target+animals+%22Nordic+Council+of+Ministers%22+Laakso&ots= Fisher, P., Griffiths, R., Speedy, C., Broome, K., 2011. Environmental monitoring for Dbt3clSK8j&sig=OnTiYefiMyu71GxmJzGrKGlSjmo#v=onepage&q=Literature% brodifacoum residues after aerial application of baits for rodent eradication. In: 20review%20on%20residues%20of%20anticoagulant%20rodenticides%20in%20non- Veitch, C.R., Clout, M.N., Towns, D.R. (Eds.), Island Invasives: Eradication and Manage- target%20animals%20%22Nordic%20Council%20of%20Ministers%22%20Laakso&f= ment. IUCN, Gland, Switzerland :pp. 300–304. http://www.issg.org/pdf/publications/ false (Available, accessed January 21, 2017). Island_Invasives/pdfHQprint/3FisherP.pdf (Available, accessed November 11, 2016). Langford, K.H., Reid, M., Thomas, K.V., 2013. The occurrence of second generation antico- Ford, R.G., 2006. Using beached bird monitoring data for seabird damage assessment: the agulant rodenticides in non-target raptor species in Norway. Sci. Total Environ. 450– importance of search interval. Mar. Ornithol. 34:91–98. http://www. 451, 205–208. marineornithology.org/PDF/34_2/34_2_91-98.pdf (Available, accessed February 28, Linsdale, J.M., 1931. Facts concerning the use of thallium in California to poison rodents: 2017). its destructiveness to game birds, song birds and other valuable wild life. Condor Galindo, J.C., Kendall, R.J., Driver, C.J., Lacher, T.E., 1985. The effect of methyl parathion on 33:92–106. http://sora.unm.edu/sites/default/files/journals/condor/v033n03/p0092- susceptibility of bobwhite quail (Colinus virginianus) to domestic cat predation. p0106.pdf (Available, accessed November 11, 2016). Behav. Neural. Biol. 43:21–36. https://dx.doi.org/10.1016/S0163-1047(85)91454-2 Linz, G.M., Davis, J.E., Engeman, R.M., Otis, D.L., Avery, M.L., 1991. Estimating survival of (Available, accessed March 03, 2017). bird carcasses in cattail marshes. Wildl. Soc. Bull. 19, 195–199. Giraudoux, P., Tremollières, C., Barbier, B., Defaut, R., Rieffel, D., Bernard, N., Lucot, É., Masuda, B.M., Fisher, P., Jamieson, I.G., 2014. Anticoagulant rodenticide brodifacoum de- Berny, P., 2006. Persistence of bromadiolone anticoagulant rodenticide in Arvicola tected in dead nestlings of an insectivorous passerine. N. Z. J. Ecol. 38:110–115. terrestris populations after field control. Environ. Res. 102:291–298. http://dx.doi. https://www.researchgate.net/profile/Penny_Fisher/publication/259312715_ org/10.1016/j.envres.2006.02.008. https://www.researchgate.net/profile/Patrick_ Anticoagulant_rodenticide_brodifacoum_detected_in_dead_nestlings_of_an_ Giraudoux/publication/7163161_Persistence_of_bromadiolone_anticoagulant_ insectivorous_passerine/links/0f317538f9045dad76000000.pdf (Available, accessed rodenticide_in_Arvicola_terrestris_populations_after_field_control/links/ November 11, 2016). 00b49521302d95b8b1000000.pdf Available, accessed March 22, 2017). McClelland, P.J., 2002. Eradication of Pacificrats(Rattus exulans) from Whenua Hou Na- Godfrey, M.E.R., 1985. Non-target and secondary poisoning hazards of “second genera- ture Reserve (Codfish Island), Putauhinu and Rarotoka Islands, New Zealand. In: tion” anticoagulants. Acta Zool. Fenn. 173, 209–212. Veitch, C.R., Clout, M.N. (Eds.), Turning the tide: the eradication of invasive species, Gómez-Ramírez, P., Shore, R.F., van den Brink, N.W., van Hattum, B., Bustnes, J.O., Duke, G., Proceedings of the International Conference On Eradication of Island Invasives Occa- Fritsch, C., García-Fernández, A.J., Helander, B.O., Jaspers, V., Krone, O., Martínez- sional Paper of the IUCN Species Survival Commission No. 27. IUCN SSS Invasive Spe- López, E., Mateo, R., Movalli, P., Sonne, C., 2014. An overview of existing raptor con- cies Specialist Group, Gland, Switzerland :pp. 173–181. https://portals.iucn.org/ taminant monitoring activities in Europe. Environ. Int. 67:12–21. http://ac.els-cdn. library/efiles/documents/SSC-OP-028.pdf#page=179 (Available, accessed November com/S0160412014000543/1-s2.0-S0160412014000543-main.pdf?_tid=df4c7b76- 11, 2016). N.B. Vyas / Science of the Total Environment 609 (2017) 68–76 75

McIlroy, J.C., 1983. The sensitivity of Australian animals to 1080 poison. V. The sensitivity Robertson, H.A., Colbourne, R.M., Graham, P.J., Miller, P.J., Pierce, R.J., 1999. Survival of of feral pigs, Sus scrofa, to 1080 and its implications for poisoning campaigns. Wildl. brown kiwi (Apteryx mantelli) exposed to brodifacoum poison in northland, New Res. 10, 139–148. Zealand. N. Z. J. Ecol. 23, 225–231. McIlroy, J.C., Gifford, E.J., 1991. Effects on non-target animal populations of a rabbit trail- Ruiz-Suárez, N., Henríquez-Hernández, L.A., Valerón, P.F., Boada, L.D., Zumbado, M., baiting campaign with 1080 poison. Wildl. Res. 18, 315–325. Camacho, M., Almeida-González, M., Luzardo, O.P., 2014. Assessment of anticoagulant Merton, D., Climo, G., Laboudallon, V., Robert, S., Mander, C., 2002. Alien mammal eradica- rodenticide exposure in six raptor species from the Canary Islands (Spain). Sci. Total tion and quarantine on inhabited islands in the Seychelles. In: Veitch, C.R., Clout, M.N. Environ. 485–486, 371–376. (Eds.), Turning the Tide: the Eradication of Invasive Species, Proceedings of the Inter- Salmon, T., Sheffield, S., Paul, E., 2010. The Rat Island rat Eradication Project: A Critical national Conference on Eradication of Island Invasives Occasional Paper of the IUCN Evaluation of Nontarget Mortality. The Ornithological Council, Bethesda, Maryland, Species Survival Commission No. 27. IUCN SSS Invasive Species Specialist Group, U.S.A., p. 85. Gland, Switzerland :pp. 182–198. http://issg.org/database/species/reference_files/ Sánchez-Barbudo, I.S., Camarero, P.R., Mateo, R., 2012. Primary and secondary poisoning TurTid/Merton.pdf (Available, accessed November 11, 2016). by anticoagulant rodenticides of non-target animals in Spain. Sci. Total Environ. Morgan, D.R., Wright, G.R., Ogilvie, S.C., Pierce, R., Thomson, P., 1996. Assessment of the 420:280–288. https://www.researchgate.net/profile/Rafael_Mateo/publication/ environmental impact of brodifacoum during rodent eradication operations in New 221824755_Primary_and_secondary_poisoning_by_anticoagulant_rodenticides_of_ Zealand. In: Timm, R.M., Crabb, A.C. (Eds.), Proceedings of the Seventeenth Vertebrate non-target_animals_in_Spain/links/00b7d53882f0337102000000.pdf (Available, Pest Conference 1996 :pp. 213–218. http://digitalcommons.unl.edu/cgi/viewcontent. accessed November 11, 2016). cgi?article=1037&context=vpc17 (Available, accessed November 11, 2016). Sarabia, J., Sánchez-Barbudo, I., Siqueira, W., Mateo, R., Rollán, E., Pizarro, M., 2008. Lesions Morriss, G.A., Nugent, G., Whitford, J., 2016. Dead birds found after aerial poisoning oper- associated with the plexus venosus subcutaneus collaris of pigeons with ations targeting small mammal pests in New Zealand 2003–14.N.Z.J.Ecol.40: chlorophacinone toxicosis. Avian Dis. 52:540–543. http://dx.doi.org/10.1637/1933- 361–370. http://dx.doi.org/10.20417/nzjecol.40.39 (Available, accessed November 5334(2008)3[e30:lawtpv]2.0.co;2 (//www.researchgate.net/profile/Rafael_Mateo/ 11, 2016). publication/23402699_Lesions_associated_with_the_plexus_venosus_subcutaneus_ Nordström, K., Kaj, L., Brorström Lundén, E., 2013. Screening 2012 Rodenticides. Swedish collaris_of_pigeons_with_chlorophacinone_toxicosis/links/ Environmental Research Institute. :p. 19. http://www.diva-portal.org/smash/get/ 02e7e53a9bd7a553d4000000.pdf. Available, accessed November 11, 2016). diva2:711711/FULLTEXT01.pdf (Available, accessed March 02, 2017). Savarie, P.J., 1981. The nature, modes of action, and toxicity of rodenticides, volume 2. In: Olea, P.P., Sánchez-Barbudo, I.S., Viñuela, J., Barja, I., Mateo-Tomás, P., Piñeiro, A., Mateo, Pimentel, D. (Ed.), CRC Handbook of Pest Management in Agriculture. CRC Press. Boca R., Purroy, F.J., 2009. Lack of scientific evidence and precautionary principle in mas- Raton, Florida, pp. 589–598. sive release of rodenticides threatens biodiversity: old lessons need new reflections. Shivaprasad, H.L., Galey, F., 2001. Diphacinone and zinc phosphide toxicity in a flock of Environ. Conserv. 36:1–4. https://www.researchgate.net/profile/Pedro_Olea/ peafowl. Avian Pathol. 30, 599–603 (//doi.org/10.1080/03079450120092080. Avail- publication/230582967_Lack_of_scientificevidence_and_precautionary_principle_ able accessed November 11, 2016). in_massive_release_of_rodenticides_threatens_biodiversity_old_lessons_need_new_ Smallwood, K.S., 2007. Estimating wind turbine–caused bird mortality. J. Wildl. Manag. reflections/links/0fcfd5040eff4641df000000.pdf (Available, accessed November 11, 71, 2781–2791. 2016). Spurr, E.B., 1993. Feeding by captive rare birds on baits used in poisoning operations for Peterson, C.A., Lee, S.L., Elliott, J.E., 2001. Scavenging of waterfowl carcasses by birds control of brushtail possums. N. Z. J. Ecol. 17, 13–18 (http://newzealandecology.org/ in agricultural fields of British Columbia. J. Field Ornithol. 72:150–159. http://dx. system/files/articles/NZJEcol17_1_13.pdf. Available, [accessed March 03, 2017]). doi.org/10.1648/0273-8570-72.1.150 (Available, accessed March 16, 2017). Spurr, E.B., 1994. Review of the impacts on non-target species of sodium Pierce, R.J., Montgomery, P.J., 1992. The fate of birds and selected invertebrates during a monofluoroacetate (1080) in baits used for brushtail possum control in New Zealand. 1080 operation. Science and Research Internal Report 121. New Zealand Department In: Seawright, A.A., Eason, C.T. (Eds.), Proceedings of the Science Workshop on 1080. of Conservation :p. 17. http://www.doc.govt.nz/Documents/science-and-technical/ The Royal Society of New Zealand Miscellaneous Series 28, pp. 124–133. ir121.pdf (Available, accessed November 11, 2016). Spurr, E.B., 2000. Impacts of possum control on non-target species. In: Montague, T.L. Pitt, W.C., Berentsen, A.R., Shiels, A.B., Volker, S.F., Eisemann, J.D., Wegmann, A.S., Howald, (Ed.), The Brushtail Possum: The Biology, Impact and Management of an Introduced G.R., 2015. Non-target species mortality and the measurement of brodifacoum roden- Marsupial. Manaaki Whenua Press. Lincoln, New Zealand, pp. 175–186. ticide residues after a rat (Rattus rattus) eradication on Palmyra Atoll, tropical Pacific. Spurr, E.B., Drew, K.W., 1999. Invertebrates feeding on baits used for vertebrate pest con- Biol. Conserv. 185:36–46. http://dx.doi.org/10.1016/j.biocon.2015.01.008 (http:// trol in New Zealand. N. Z. J. Ecol. 23, 167–173 (//www.researchgate.net/profile/Jay_ digitalcommons.unl.edu/cgi/viewcontent.cgi?article=2711&context=icwdm_ McCartney/publication/248911597_Forest_invertebrates_found_on_baits_used_in_ usdanwrc. Available, accessed November 11, 2016). pest_mammal_control_and_the_impact_of_sodium_monofluoroacetate_(1080)_on_ Poppenga, R.H., Ziegler, A.F., Habecker, P.L., Singletary, D.L., Walter, M.K., Miller, P.G., 2005. their_numbers_at_Ohakune_North_Island_New_Zealand/links/ Zinc phosphide intoxication of wild turkeys (Meleagris gallopavo). J. Wildl. Dis. 41, 00b7d52df566269efb000000.pdf. Available, [accessed November 11, 2016]). 218–223 (//doi.org/10.7589/0090-3558-41.1.218. Available, accessed November 11, Spurr, E.B., Powlesland, R.G., 1997. Impacts of aerial application of 1080 on non-target na- 2016). tive fauna. Science for Conservation (Wellington, NZ). 62, p. 20 (http:// Powlesland, R.G., Knegtmans, J.W., Marshall, I.S.J., 1999. Costs and benefits of aerial 1080 nationalparks.co.nz/Documents/science-and-technical/Sfc062.pdf. Available, possum control operations using carrot baits to North Island robins (Petroica australis accessed November 11, 2016). longipes), Pureora Forest Park. N. Z. J. Ecol. 23:149–159. http://www.lincoln.ac.nz/ Spurr, E.B., Maitland, M.J., Taylor, G.E., Wright, G.R.G., Radford, C.D., Brown, L.E., 2005. Res- PageFiles/7074/3474_Powleslandetal__s10663.pdf (Available, accessed November idues of brodifacoum and other anticoagulant pesticides in target and non-target spe- 11, 2016). cies, Nelson Lakes National Park, New Zealand. N. Z. J. Zoology 32, 237–249 //doi.org/ Powlesland, R.G., Knegtmans, J.W., Styche, A., 2000. Mortality of North Island tomtits 10.1080/03014223.2005.9518416. Available [accessed November 11, 2016]. (Petroica macrocephala toitoi) caused by aerial 1080 possum control operations, Spurr, E.B., Foote, D., Lindsey, G.D., Perry, C.F., 2015. Arial-broadcast application of 1997-98, Pureora Forest Park. N. Z. J. Ecol.:161–168. http://citeseerx.ist.psu.edu/ diphacinone bait for rodent control in Hawaii: efficacy and non-target species risk as- viewdoc/download?doi=10.1.1.376.840&rep=rep1&type=pdf (Available, accessed sessment. Technical Report HCSU-071. Hawaii Cooperative Studies Unit, p. 28 (http:// November 20, 2016). dspace.lib.hawaii.edu/bitstream/10790/2650/1/TR071FooteBait.pdf. Available, Proulx, G., 2011. Field evidence of non-target and secondary poisoning by strychnine [accessed March 03, 2017]). and chlorophacinone used to control Richardson’s ground squirrels in southwest Statham, M., 2005. The development of 1080 use for rabbit control in Tasmania. Papers Saskatchewan. In: Danyluk, D. (Ed.), Patterns of Change. Proceedings of the and Proceedings of the Royal Society of Tasmania. 139, pp. 1–6(http:// Ninth Prairie Conservation and Endangered Species Conference 2010, Winnipeg, eprints.utas.edu.au/13363/1/2005-statham-development-1080.pdf. Available, Manitoba, Canada :pp. 128–134. http://alphawildlife.ca/wp-content/uploads/ accessed November 11, 2016). 2015/03/108-2011-Field-evidence-PCESC-proceedings.pdf (Available, accessed Stone, W.B., Okoniewski, J.C., Stedelin, J.R., 1999. Poisoning of wildlife with anticoagulant ro- November 11, 2016). denticides in New York. J. Wildl. Dis. 35, 187–193 (http://www.bioone.org/doi/pdf/ Proulx, G., 2014. On the misuse of pesticides to control northern pocket gophers and 10.7589/0090-3558-35.2.187. Available, accessed March 03, 2017). Richardson’s ground squirrels in agriculture and the pressing need for sustainable so- Swenson, J., Bradley, G.A., 2013. Suspected cholecalciferol rodenticide toxicosis in avian lutions. In: Holroyd, G.L., Trefry, A.J., Crockett, B. (Eds.), Engaging People in Conserva- species at a zoological institution. J. Avian Med. Surg. 27, 136–147. tion, Proceedings of the 10th Prairie Conservation and Endangered Species 2013, Red Sztukowski, L.A., Kesler, D.C., 2013. Bait Consumption by Sooty Terns: Implications for Is- Deer, Alberta, Canada :pp. 134–157. http://pcesc.ca/media/8212/pcesc_proceedings_ land Eradication Programmes. 23. Bird Conservation International, pp. 36–44. 2014-09-19_for_web.pdf#page=134 (Available, accessed November 11, 2016). Taylor, D.P., 1984. Identification and Detection of the Rats in New Zealand and the Erad- Pryde, M.A., Pickerell, G., Coats, G., Hill, G.S., Greene, T.C., Murphy, E.C., 2013. Observations ication of Ship Rats on Tawhitinui Island. Dissertation, Lincoln College, Cantebury, of South Island robins eating Racumin®, a toxic paste used for rodent control. N. Z. New Zealand. p. 73 (//researcharchive.lincoln.ac.nz/bitstream/handle/10182/5083/ J. Zoology 40, 255–259. taylor_dipp&r.pdf?sequence=5. Available, [accessed November 11, 2016]). Ramey, C.A., Sterner, R.T., 1995. Mortality of gallinaceous birds associated with 2% zinc Taylor, R.H., Thomas, B.W., 1993. Rats eradicated from rugged Breaksea Island (170 ha), phosphide baits for control of voles in alfalfa. Int. Biodeterior. Biodegrad. 36, 51–64. Fiordland, New Zealand. Biol. Conserv. 65, 191–198. Record, C.R., Marsh, R.E., 1988. Rodenticide residues in animal carcasses and their rele- Thomas, P.J., Mineau, P., Shore, R.F., Champoux, L., Martin, P.A., Wilson, L.K., Fitzgerald, G., vance to secondary hazards. In: Crabb, A.C., Marsh, R.E. (Eds.), Proceedings Thirteenth Elliott, J.E., 2011. Second generation anticoagulant rodenticides in predatory birds: Vertebrate Pest Conference 1988, Monterey, California, U.S.A. :pp. 163–168. http:// probabilistic characterization of toxic liver concentrations and implications for pred- digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1033&context=vpcthirteen atory bird populations in Canada. Environ. Int. 37, 914–920. (Available, accessed November 11, 2016) Torr, N., 2002. Eradication of rabbits and mice from subantarctic Enderby and Rose Ritz, B., Tager, I., Balmes, J., 2005. Can lessons from public health disease surveillance be Islands. In: Veitch, C.R., Clout, M.N. (Eds.), Turning the tide: the eradication of invasive applied to environmental public health tracking. Environ. Health Perspect. 113: species, Proceedings of the International Conference On Eradication of Island Inva- 243–249. http://infohouse.p2ric.org/ref/52/51496.pdf (Available, accessed April 17, sives Occasional Paper of the IUCN Species Survival Commission No. 27. IUCN SSS In- 2016). vasive Species Specialist Group, Gland, Switzerland:pp. 319–328 (https://portals. 76 N.B. Vyas / Science of the Total Environment 609 (2017) 68–76

iucn.org/library/efiles/documents/SSC-OP-028.pdf#page=179. Available, [accessed Conference On Eradication of Island Invasives Occasional Paper of the IUCN Species November 11, 2016]). Survival Commission No. 27. IUCN SSS Invasive Species Specialist Group, Gland, Swit- Tosh, D.G., Shore, R.F., Jess, S., Withers, A., Bearhop, S., Montgomery, W.I., McDonald, R.A., zerland, pp. 353–356 (//portals.iucn.org/library/efiles/documents/SSC-OP- 2011. User behaviour, best practice and the risks of non-target exposure associated 028.pdf#page=359. Available, [accessed March 03, 2017]). with anticoagulant rodenticide use. J. Environ. Manag. 92, 1503–1508. Veltman, C.J., Westbrooke, I.M., 2011. Forest bird mortality and baiting practices in New Towns, D.R., McFadden, I., Lovegrove, T., 1993. Offshore Islands co-Operative Conservation Zealand aerial 1080 operations from 1986 to 2009. N. Z. J. Ecol. 35, 21–29 (http:// Project with ICI Crop Care Division: Phase One (Stanley Island) Science & Research In- newzealandecology.org/system/files/articles/NZJEcol35_1_21.pdf. Available, ternal Report No. 138. Department of Conservation, Wellington, New Zealand, p. 24 [accessed November 11, 2016]). (http://www.doc.govt.nz/Documents/science-and-technical/SRIR138.pdf. Available, Vogt, R.L., LaRue, D., Klaucke, D.N., Jillson, D.A., 1983. Comparison of an active and passive [accessed April 1, 2017]). surveillance system of primary care providers for hepatitis, measles, rubella, and sal- US EPA U.S. Environmental Protection Agency, 2008. Risk Mitigation Decision for Ten Ro- monellosis in Vermont. Am. J. Public Health 73, 795–797 (10.2105/ajph.73.7.795. denticides (//www.regulations.gov/document?D=EPA-HQ-OPP-2006-0955-0764. Available, accessed November 11, 2016). Available, [accessed November 19, 2016]). Vyas, N.B., 1999. Factors influencing estimation of pesticide-related wildlife mortality. US EPA United States Environmental Protection Agency, 1998. Rodenticide Cluster Regis- Toxicol. Ind. Health 15, 187–192 (http://citeseerx.ist.psu.edu/viewdoc/download? tration Eligibility Decision. https://nepis.epa.gov/Exe/ZyNET.exe/20000OOQ.TXT? doi=10.1.1.841.7647&rep=rep1&type=pdf. Available, accessed November 11, 2016). ZyActionD=ZyDocumentandClient=EPAandIndex=1995+Thru+1999andDocs= Vyas, N.B., 2013. Untested pesticide mitigation requirements: ecological, agricultural, and andQuery=andTime=andEndTime=andSearchMethod=1andTocRestrict= legal implications. Drake J. Agric. Law 18.2, 335–348 (http://students.law.drake.edu/ nandToc=andTocEntry=andQField=andQFieldYear=andQFieldMonth= agLawJournal/docs/agVol18No2-Vyas.pdf. Available, [accessed November 11, 2016). andQFieldDay=andIntQFieldOp=0andExtQFieldOp=0andXmlQuery=andFile=D% Vyas, N.B., Hulse, C.S., Meteyer, C.U., Rice, C.P., 2013. Evidence of songbird intoxication 3A%5Czyfiles%5CIndex%20Data%5C95thru99%5CTxt%5C00000011%5C20000OOQ. from Rozol® application at a black-tailed prairie dog colony. J. Fish Wildl. Manag. 4, txtandUser=ANONYMOUSandPassword=anonymousandSortMethod=h%7C- 97 –103 (//doi.org/10.3996/052012-jfwm-042. Available, accessed November 11, andMaximumDocuments=1andFuzzyDegree=0andImageQuality=r75g8/r75g8/ 2016). x150y150g16/i425andDisplay=hpfrandDefSeekPage=xandSearchBack= Vyas, N.B., Kuncir, F., Clinton, C.C., 2017. Influence of poisoned prey on foraging behavior ZyActionLandBack=ZyActionSandBackDesc=Results%20pageandMaximumPages= of ferruginous hawks. Am. Midl. Nat. 177:75–83. http://dx.doi.org/10.1674/0003- 1andZyEntry=1andSeekPage=xandZyPURL (Available, [accessed November 11, 0031-177.1.75 (Available, accessed March 02, 2017). 2016]). Walker, L.A., Chaplow, J.S., Moeckel, C., Pereira, M.G., Potter, E.D., Shore, R.F., 2015. Antico- Veitch, C.R., 2002a. Eradication of Pacificrats(Rattus exulans) from Tiritiri Matangi Island, agulant Rodenticides in Sparrowhawks: A Predatory Bird Monitoring Scheme (PBMS) Hauraki Gulf, New Zealand. In: Veitch, C.R., Clout, M.N. (Eds.), Turning the tide: the report. Centre for Ecology and Hydrology, Lancaster, U.K., p. 12 (http:// eradication of invasive species, Proceedings of the International Conference On Erad- nora.nerc.ac.uk/511023/1/N511023CR.pdf. Available, accessed November 11, 2016). ication of Island Invasives Occasional Paper of the IUCN Species Survival Commission Ward, M.R., Stallknecht, D.E., Willis, J., Conroy, M.J., Davidson, W.R., 2006. Wild bird mor- No. 27. IUCN SSS Invasive Species Specialist Group, Gland, Switzerland, pp. 360–364 tality and West Nile virus surveillance: biases associated with detection, reporting, (//portals.iucn.org/library/sites/library/files/documents/ssc-op-028.pdf#page=366. and carcass persistence. J. Wildl. Dis. 42, 92–106 (//doi.org/10.7589/0090-3558- Available, [accessed March 03, 2017]). 42.1.92. Available, accessed November 11, 2016). Veitch, C.R., 2002b. Eradication of Norway rats (Rattus norvegicus) and house mouse (Mus Zeakes, S.J., Hansen, M.F., Robel, R.J., 1981. Increased susceptibility of bobwhites (Colinus musculus) from Motuihe Island, New Zealand. In: Veitch, C.R., Clout, M.N. (Eds.), virginianus)toHistomonas meleagridis after exposure to Sevin insecticide. Avian Dis. Turning the tide: the eradication of invasive species, Proceedings of the International 25, 981–987.