DOI: 10.7589/2013-07-160 Journal of Wildlife Diseases, 51(1), 2015, pp. 000–000 # Wildlife Disease Association 2015

NONTARGET MORTALITY OF NEW ZEALAND LESSER SHORT-TAILED BATS (MYSTACINA TUBERCULATA) CAUSED BY DIPHACINONE

Gillian C. Dennis1,2,3 and Brett D. Gartrell2 1 Ecology Group, Institute of Agriculture and Environment, Massey University, Private Bag 11222, Palmerston North, New Zealand 2 Wildbase, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11222, Palmerston North, New Zealand 3 Corresponding author (email: [email protected])

ABSTRACT: Primary and secondary poisoning of nontarget wildlife with second-generation anticoagulant rodenticides has led to restrictions on their use and to increased use of first- generation anticoagulants, including diphacinone. Although first-generation anticoagulants are less potent and less persistent than second-generation compounds, their use is not without risks to nontarget species. We report the first known mortalities of threatened New Zealand lesser short- tailed bats (Mystacina tuberculata) caused by diphacinone intoxication. The mortalities occurred during a rodent control operation in Pureora Forest Park, New Zealand, during the 2008–2009 Austral summer. We observed 115 lesser short-tailed bat deaths between 9 January and 6 February 2009, and it is likely that many deaths were undetected. At necropsy, adult bats showed gross and histologic hemorrhages consistent with coagulopathy, and diphacinone residues were confirmed in 10 of 12 liver samples tested. The cause of mortality of pups was diagnosed as a combination of the effects of diphacinone toxicity, exposure, and starvation. Diphacinone was also detected in two of 11 milk samples extracted from the stomachs of dead pups. Eight adults and 20 pups were moribund when found. Two adults and five pups survived to admission to a veterinary hospital. Three pups responded to treatment and were released at the roost site on 17 March, 2009. The route of diphacinone ingestion by adult bats is uncertain. Direct consumption of toxic bait or consumption of poisoned arthropod prey could have occurred. We suggest that the omnivorous diet and terrestrial feeding habits of lesser short-tailed bats make them susceptible to poisoning with the bait matrix and the method of bait delivery used. We recommend the use of alternative vertebrate pesticides, bait matrices, and delivery methods in bat habitat. Key words: Anticoagulant rodenticides, conservation, microchiroptera, Mystacinidae, pathology, pest control, toxicants, wildlife.

INTRODUCTION compounds. Both types act by interfering with the synthesis of vitamin K-dependent Anticoagulant rodenticides are com- blood clotting factors in the liver of monly used to control rodent pests in vertebrates, causing fatal hemorrhaging urban and agricultural settings worldwide; (Buckle 1994). Second-generation com- they are also widely used to eradicate pounds are more potent and more persis- introduced rodents from mammal-free tent in animal tissue than are first- island ecosystems for conservation pur- generation compounds (Fisher et al. poses (Towns and Broome 2003; Howald 2003; Erickson and Urban 2004), increas- et al. 2007). In New Zealand, where the ing the risk of poisoning of nontarget only native land mammals are two species animals by direct consumption of poi- of bats (King 2005), these pesticide soned bait (primary exposure) or by compounds are also used to control rats consumption of poisoned prey (secondary (Rattus spp.) in mainland conservation exposure) (Eason and Spurr 1995). Mor- reserves using broad-scale, sustained, talities and sublethal poisonings, caused ground-based applications (Innes and through both primary and secondary Barker 1999). routes of exposure to second-generation Anticoagulant rodenticides are catego- compounds, have been recorded for a rized as either first- or second-generation wide range of nontarget bird (e.g., Eason

0 0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015 et al. 2002) and mammal species (e.g., therefore been considered vulnerable to Fournier-Chambrillon et al. 2004). Intox- primary poisoning through consumption of ication of nontarget wildlife with first- toxic baits encountered while foraging generation compounds also occurs (e.g., (Eason and Spurr 1995) or to secondary Stone et al. 1999) but much less frequent- poisoning by consumption of arthropods ly (Erickson and Urban 2004). that had fed on toxic bait (Lloyd and Widespread concern about the continu- McQueen 2000; Craddock 2003). ing impacts of second-generation antico- This is the first reported case of lesser agulant rodenticides on nontarget wildlife short-tailed bat deaths due to anticoagu- has led to new restrictions on their use lant poisoning. The incident occurred (Department of Conservation 2000; US during a rodent control operation in native Environmental Protection Agency 2008) forest on public conservation land in New and to the investigation of more-suitable Zealand in January 2009. The mortalities first-generation compounds, including di- were detected at two roost trees during phacinone. Diphacinone has been consid- the bats’ breeding season (November– ered a promising alternative to second- February) when pups are born and generation compounds because it has cre`ched in maternity roosts. We docu- medium potency to rodents but relatively mented the mortality event and subse- short persistence in animal tissue (Fisher quent investigation to provide records for et al. 2003). In New Zealand diphacinone future reference. has proven effective for controlling rats in mainland conservation reserves (Gillies MATERIALS AND METHODS et al. 2006). In the USA it is used to Study site control rodents in commensal (Erickson and Urban 2004), agricultural, and range- The bat mortalities occurred in Pikiariki Ecological Area, Pureora Forest Park, in land settings (Salmon et al. 2007) and to the North Island, New Zealand (38u319S, eradicate rodents from small islands for 175u349E). Pikiariki Ecological Area (hereafter conservation purposes (Witmer et al. ‘‘Pikiariki’’) is a remnant of old-growth, native 2007b). podocarp-hardwood forest (457 ha) within Although less potent and less persistent Pureora Forest Park (78,000 ha). Pikiariki has been designated an Ecological Area in than second-generation anticoagulants, recognition of its high conservation values and the use of diphacinone is not without provides the core breeding and colonial roost ecologic risk (Eisemann and Swift 2006; tree habitat for a population of lesser short- Rattner et al. 2012). Secondary poisoning tailed bats. of raptors that were fed mice killed with Bat mortalities diphacinone has been demonstrated in laboratory trials (Mendenhall and Pank On January 9, 2009, dead and moribund lesser short-tailed bats were discovered at the 1980), and residues of diphacinone have bases of a maternity roost tree and a nearby been detected in wild populations of colonial roost tree. At the time, a rodent nontarget birds (e.g., Stone et al. 2003), control operation using diphacinone (0.005%) invertebrates (e.g., Johnston et al. 2005), was taking place in Pikiariki to limit the roof and mammals (e.g., Riley et al. 2007). rat (Rattus rattus) population. The active ingredient was presented in a cereal paste We report nontarget mortalities of New matrix (RatAbateH, Connovation Ltd., Auck- Zealand lesser short-tailed bats (Mystacina land, New Zealand) and delivered in biode- tuberculata) due to diphacinone intoxica- gradable plastic bait bags, each containing tion. These threatened, endemic bats have 300 g of paste. Bait bags were stapled to tree a terrestrial foraging habit and a broad diet trunks 0.2–1 m above the ground on a 150 3 50-m grid throughout Pikiariki. Baiting com- comprising terrestrial, arboreal, and aerial menced on 21 October 2008, with subsequent arthropods, nectar, pollen, and fruit (Dan- bait deployments in November and December iel 1976; Arkins et al. 1999). They have to maintain availability to rodents. DENNIS AND GARTRELL—DIPHACINONE TOXICITY IN NEW ZEALAND SHORT-TAILED BATS 0

Daily checks for further mortalities at the two roost trees continued for 34 d. An additional eight known colonial and maternity roost trees were also monitored for signs of occupancy and for mortalities. We attempted to locate any unknown roost trees which might have been occupied. Eight adult bats in apparent good health were captured in mist nets (38 mm, Avinet, City, State, USA) and fitted with radio transmitters (BD2A, Holohil Systems, Carp, Ontario, Canada), attached between the scapulae on an area of partially trimmed fur, using a latex-based contact adhesive (Ados F2H, CRC Industries New Zealand, Auckland, New Zealand). Transmit- FIGURE 1. Numbers of dead and moribund ters weighed #0.7 g and represented ,5% of lesser short-tailed bat (Mystacina tuberculata) adults bat body mass. Bats were radio-tracked to and pups recovered each day over a 29-d period from roosts during the day using a hand-held TR4 beneath an active maternity roost tree and a nearby receiver (Telonics, Mesa, Arizona, USA) and a colonial roost tree in Pureora Forest Park, New hand-held, 3-element Yagi aerial (Sirtrack, Zealand, during a large mortality event in 2009. The Havelock North, New Zealand). Intensive large number of bats recovered on day 1 reflects an monitoring of the affected roosts continued accumulation of bat bodies over an unknown period for 5 d after the last casualty was found. The of time prior to discovery. Intensive monitoring of diphacinone-laced baits were removed from the affected roost trees continued for 5 d beyond the the field within 4 d of finding the first dead bats, last bat recovery on day 29. following the preliminary necropsy findings. treatment. Admitted bats were initially hydrat- Pathology ed twice daily with warmed subcutaneous fluids (0.9% NaCl/2.5% glucose) and dosed Dead bats were chilled and transported to with subcutaneous vitamin K (Konakion, Massey University, Palmerston North, New Roche, Auckland, New Zealand) at 10 mg/kg. Zealand. Those in suitable condition were Bats then received 10 mg/kg oral vitamin K necropsied. Tissue samples were fixed in 10% solution twice a day, prepared by a com- neutral buffered formalin. Fixed tissues were pounding pharmacist. Treatment with vitamin embedded in paraffin, sectioned at 4 mm, and K continued for 34 d. General rehabilitation stained with hematoxylin and eosin for histo- continued for a further 3 wk. logic examination. Fresh tissue samples of lung, liver, and kidney were taken from adults and pups for aerobic bacterial culture. Stom- RESULTS ach contents of freshly dead adults were Mortality, morbidity, and response to treatment examined. Pup stomachs containing milk were excised and frozen. We collected 118 affected bats from two roost sites over 29 d (Fig. 1). Recovery of Toxicology dead and moribund adults (n547 and 8, Liver samples were frozen separately for respectively) and nonvolant pups (n543 toxicologic analysis. The diphacinone content dead and 20 moribund) included both of selected liver samples and maternal milk 5 extracted from the stomachs of pups was sexes (n 39 males, 29 females, and 50 determined by high-performance liquid chro- unknown). Most affected bats were locat- matography. The method detection limit was ed on the ground within approximately 3 m 0.05 mg/g for liver and was undetermined for of the base of the maternity roost tree. milk. The uncertainty (95% CI) was 620%. One moribund and two dead adult bats Assays were performed by CENTOX (Centre for Environmental Toxicology), Landcare Re- were located at the base of a colonial roost search, Lincoln, New Zealand. tree 65 m east of the maternity roost. The maternity roost remained active through- Treatment of live bats out the monitoring period. No mortalities Moribund bats were given supportive care or injured bats were detected at an and transported to Massey University for additional eight known maternity and 0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015 colonial roosts, and no new colonial or TABLE 1. Location and incidence of hemorrhagic maternity roosts were identified through lesions in lesser short-tailed bat (Mystacina tuberculata) adults and pups with diphacinone radio-tracking of eight tagged adult bats. toxicity, as determined at necropsy by gross and Affected bats found alive were lethargic histologic examination, New Zealand, 2009. and did not resist handling. Four mori- bund adults and nine moribund pups died No. of bats shortly after collection. The remaining Site of hemorrhage Adults (n511) Pups (n516) four adults and 11 pups found alive were Subcutaneous 4 15 transported to Massey University. Two Peritoneal cavity 5 5 adults and five pups survived to admission. Lungs 6 3 Three pups were successfully treated and Heart 3 0 were released at the roost site on 17 Skeletal muscle 2 0 March, 2009. Meninges 1 0 Liver 1 0 Perineal region 1 0 Pathology findings Dead bats were in various stages of decomposition, ranging from intact to The stomachs of six dead adult bats desiccated specimens, indicating that the contained pollen and arthropod frag- mortalities had occurred over several days ments. None contained evidence of cereal to weeks. Subcutaneous bruising and hem- bait consumption. Forty dead pups were orrhage on the abdomen, neck, thorax, legs, in suitable condition for examination of and around the bones of the wings was the abdominal organs. Twenty-two pups noted on external examination of some of had an empty stomach, 17 stomachs the fresher specimens, particularly on contained milk, and one contained pollen unfurred pups. There was dried blood in and arthropod fragments. Six of the milk the mouth of one dead adult bat and around samples may have been bat milk formula the anus of another, but no moribund bats that pups received while in care, and these exhibited signs of external bleeding. were excluded from toxicologic analysis. Eleven adults and 16 pups were in The remaining 11 samples were maternal suitable condition for necropsy. At nec- milk. ropsy, one adult and four pups that died Histopathologic examination shortly after collection were in poor body condition. Two of these pups were severe- Histopathologic findings in five of eight ly dehydrated, as evidenced by skin turgor adults and three of seven pups examined and tacky serosal surfaces. The most were indicative of coagulopathy. Signifi- frequently observed necropsy findings cant lesions in adults included recent were subcutaneous hemorrhages, hemo- hemorrhage in the myocardium and peri- peritoneum, and pulmonary hemorrhage cardium (n52), in the pleura or alveoli of (Table 1). Subcutaneous hemorrhages the lung (n54), in the peritoneum and the were observed in a variety of locations serosal surfaces of abdominal viscera on both adults and pups. In two adults (n52), and in the intestinal muscular wall internal hemorrhaging was severe. There (n51). Significant lesions in pups included were no skeletal fractures that might atelectasis in some areas of the lung indicate trauma as a cause of hemorrhage. (n51), diffuse moderate accumulations One adult and nine pups showed no of hemosiderin in the cytoplasm of hepa- evidence of internal hemorrhaging. Only tocytes (n52), free erythrocytes in the one pup showed no evidence of any stomach lumen (n51), hemorrhage within hemorrhaging. Pallor of the liver was the lumen of the alveoli (n51), and large, observed in one adult and one pup and recent hemorrhages on the serosa of the pallor of the lungs in one pup. kidney (n51). DENNIS AND GARTRELL—DIPHACINONE TOXICITY IN NEW ZEALAND SHORT-TAILED BATS 0

Microbiology dosed with 3 mg/kg diphacinone) (Eason Ten species of bacteria were cultured and Wickstrom 2001). It is likely, there- from samples of liver, lung, and kidney fore, that the live bats which allowed us to from short-tailed bat adults (n53) and approach and handle them were already pups (n51); Corynebacterium sp. (n53 severely affected by diphacinone. Further- bats), Proteus sp. (n52), alpha hemolytic more stress, caused by handling and Streptococcus sp. (n52), nonhemolytic transport, could have exacerbated suscep- Streptococcus sp. (n52), Micrococcus sp. tibility to anticoagulant toxicosis (Robin- (n51), Staphylococcus aureus (n51), son et al. 2005). Escherichia coli (n51), Proteus mirabilis The cause of mortality of bat pups was (n51), Hafnia alvei (n51), and Serratia diagnosed as a combination of the effects sp. (n51). None of the bacteria isolated of diphacinone toxicity, exposure, and was considered to be a primary pathogen. starvation. The presence of diphacinone in the maternal milk collected from the Toxicology stomachs of dead pups provided evidence Diphacinone was confirmed in liver that the poison was passed from lactating samples from four of five adults (mean adult females to their pups. This route of concentration6SE; 0.2960.06 mg/g, n54) intoxication with pesticides has been and six of seven pups tested (0.3260.07 mg/ reported for bat pups in the USA (e.g., g, n56). Concentrations ranged from 0.19 Clark et al. 1978, 1988). The pathway of to 0.68 mg/g of liver tissue. Diphacinone diphacinone intoxication of the adult bats was also confirmed in two of the 11 at Pikiariki, however, is uncertain. maternal milk samples tested at concen- Route of exposure trations of 0.23 and 0.09 mg/g. Two likely routes of exposure of adult DISCUSSION bats to diphacinone at Pikiariki are direct consumption of toxic bait or secondary Cause of death poisoning after eating arthropods that had Our investigation confirms a diagnosis of consumed toxic bait. Due to the delayed diphacinone-induced coagulopathy of less- mode of action of anticoagulants and the er short-tailed bats. Diagnosis was support- rapid gut transit time of microbats (Klite ed by a history of exposure, clinical signs, 1965), the absence of bait in the stomachs gross and histologic lesions at necropsy, of examined adult bats does not exclude toxicologic analysis, and response to treat- the possibility of primary poisoning. ment. For 80 d leading up to the observed Themethodofpresentationofthe mortalities, diphacinone-laced baits were diphacinone-laced baits during the mor- distributed throughout the bats’ core roost- tality event may have increased the ing habitat. Diphacinone residues were potential for bait encounters and con- confirmed in liver samples from both adults sumption by foraging adult bats. Diphaci- and pups and in two samples of maternal none was formulated in cereal paste baits milk. Severe diffuse hemorrhage, as ob- which were placed in biodegradable bags served in the bats at the time of necropsy, is stapled to tree trunks rather than in characteristic of anticoagulant poisoning pelletized cereal baits secured in bait (Berny 2007). stations. Bait acceptance trials indicate Few of the affected bats which were that captive lesser short-tailed bats are recovered alive during the mortality event unlikely to consume the pelletized cereal survived for more than a few days after baits typically used in vertebrate pest collection. Following ingestion of a lethal control operations (Lloyd 1994). However, dose of an anticoagulant, there is a delay in a separate captive trial, lesser short- of several days until death (5–6 d in rats tailed bats sampled cereal paste baits, 0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015 similar to the RatAbate paste used at cinone determined for caged (unexer- Pikiariki, although it was uncertain wheth- cised) vampire bats is 0.91 mg/kg (Thomp- er the quantities consumed were sufficient son et al. 1972) and in active bats may be to put bats at risk of poisoning (Beath et al. closer to 0.3 mg/kg (Bullard and Thomp- 2004). son 1977). Furthermore, LD50 figures for Consumption of toxic bait by arthropods acute doses of first-generation anticoagu- may have served as a pathway for second- lants are typically higher than multiple ary exposure of lesser short-tailed bats to doses administered over several consecu- diphacinone (Lloyd and McQueen 2000). tive days, suggesting that the risks associ- Pesticide-contaminated prey have been ated with the use of these compounds are implicated in mortalities of insectivorous underestimated (Vyas and Rattner 2012). bats in the USA (Clark et al. 1988; O’Shea The acute oral LD50 of diphacinone for and Clark 2002), and a wide variety of lessershort-tailedbatsisnotknown arthropod species have been observed on (Fisher and Broome 2010), and caution pelletized cereal baits in New Zealand must be observed when using data from forests (e.g., Sherley et al. 1999; Spurr and similar species to predict sensitivity (Mc- Drew 1999). Residue analysis of arthro- Ilroy 1986). pods exposed to anticoagulant baits in laboratory and field trials confirm that Extent of mortalities they may act as vectors of these com- The number of carcasses recovered in pounds (Craddock 2003; Fisher et al. Pikiariki is likely to be an underestimate of 2007). the total mortality of lesser short-tailed Despite evidence to support a secondary bats resulting from diphacinone intoxica- route of poisoning, no mortalities have tion. Carcass counts are unreliable esti- previously been detected in wild lesser mators of mortality (Vyas, 1999). The large short-tailed bat populations monitored number of decomposed bodies found on through pest control operations using the first day of recovery suggests that pelletized cereal baits laced with anticoag- deaths had been occurring for several days ulants, either when aerially broadcasted to weeks. Many adult deaths may have (Sedgeley and Anderson 2000) or con- gone undetected between initial deploy- cealed in bait stations (O’Donnell et al. ment of baits in October and the start of 2011). Further investigation into the palat- our surveillance 80 d later on January 9. ability and acceptance of a nontoxic RatA- Pups are born in late December, and so bate paste matrix to lesser short-tailed bats would have been susceptible to poisoning and forest arthropods is required. for a much-shorter period, but maternal exposure may have caused prenatal losses Sensitivity to diphacinone through abortion (Robinson et al. 2005). Species differ in their sensitivities to a During the interval between death and particular toxicant (Erickson and Urban our searches, carcasses may have decom- 2004), although there may be general posed or been removed by scavengers, and trends within animal groups (McIlroy sick animals may have been taken by 1986). The microchiroptera may be rela- predators. Furthermore, dead and mori- tively more sensitive to diphacinone than bund lesser short-tailed bats encountered are most other mammal groups. Vampire in our searches were difficult to see due to bats (Desmodus rotundus) are sensitive to their color and small size, and some bats diphacinone, and populations in Central may have been obscured from view by and South America are controlled using vegetation. An unknown number of bats this toxicant in systemic or dermal appli- may have died inside the affected roost cations (Arellano-Sota 1988). The acute trees, at other unidentified roost trees, or oral median lethal dose (LD50) of dipha- away from roost sites. DENNIS AND GARTRELL—DIPHACINONE TOXICITY IN NEW ZEALAND SHORT-TAILED BATS 0

Adult bat deaths were detected for While the use of vertebrate pesticides several days following removal of toxic remains a necessity, measures which baits from Pikiariki, most likely due to the reduce exposure to, and the adverse delayed onset of symptoms in lethally effects on, nontarget species are important dosed animals. Sublethal intoxication of (Witmer et al. 2007a; Eason et al. 2010). lactating females, or their eventual death, Determination of the route of exposure of may account for the extended period of the Pikiariki lesser short-tailed bats to pup deaths observed. The hepatic elimi- diphacinone will help inform bait design nation half-life of diphacinone is 3 d in and delivery to reduce the risk of further female laboratory rats (Fisher et al. 2003). mortalities during future rodent control If it is similar in lesser short-tailed bats, operations in bat habitat. The effective- the clotting mechanism would begin to ness of any operational changes in mini- recover 3 d after exposure and we would mizing risks to bats should be evaluated by not expect mortalities to continue long appropriate monitoring of bat populations. after bait removal. However, sublethally Until more information is available, we exposed individuals may have been affect- recommend the use of less-potent toxi- ed in ways which compromised their cants, presented in pelletized cereal baits survival beyond this period (e.g., Riley et delivered in secure bait stations, to control al. 2007; Lemus et al. 2011). vertebrate pests in bat habitat. The overall impact of the bat mortalities on the viability of the Pikiariki population ACKNOWLEDGMENTS is not known. Bats are a long-lived species We thank Department of Conservation staff with low reproductive output (Barclay and at Pureora Field Centre, Maniapoto Area Harder 2003). We lack information on Office, and Hamilton Conservancy Office for population trends and the size of the assistance during and following the mortality Pikiariki lesser short-tailed bat population event. Special thanks to Jo O’Boyle, volunteers Tanja Straka and Kahori Nakagawa, Auckland before and after the mortality event. University staff member Stuart Parsons, and There is a need for baseline data on students Eru Nathan and Victor Obolonkin for population size and long-term studies on assistance in the field, and to Stuart Parsons population dynamics to monitor the pop- and Department of Conservation scientist ulation’s recovery and viability. Colin O’Donnell for advice during the event. Thanks also to Dawne Morton of Manawatu- Management implications Wanganui Bird Rescue and volunteers from Tongariro Natural History Society for trans- These findings illustrate the hazards of port of moribund bats to Massey University. diphacinone use to the lesser short-tailed Microbial cultures were performed by New bat. However, the risks to nontarget species Zealand Veterinary Pathology. Eighty-two lesser short-tailed bat specimens recovered of anticoagulant rodenticide use should be during this study were deposited at the weighed against the benefits of control of Museum of New Zealand Te Papa Tongerewa, rodent pests (e.g., Pascal et al. 2005). The Wellington, and are stored under Accession lesser short-tailed bat, classified as vulner- Lot 3599. GCD was employed by the Depart- able by the International Union for the ment of Conservation during the mortality event and undertook subsequent investigation Conservation of Nature (O’Donnell 2008), in partial fulfilment of a Doctoral degree at is likely to benefit from rodent control Massey University, Palmerston North, New (Pryde et al. 2005). Furthermore, the Zealand. Funding support was received from consequences of failing to reduce rodent the Department of Conservation for diphaci- pest impacts can be extreme, as demon- none residue analysis of liver and milk strated by the probable extinction of the samples. GCD received personal financial support during this study from the Julie Alley New Zealand greater short-tailed bat Bursary and JP Skipworth (Ecology) Scholar- (Mystacina robusta) (Daniel 1990; Worthy ship through Massey University. This manu- 1997; O’Donnell et al. 2010). script benefited from comments by Doug 0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015

Armstrong of Massey University and Colin tives to brodifacoum and 1080 for possum and O’Donnell. rodent control—How and why? New Zeal J Zool 37:175–183. LITERATURE CITED Eason CT, Wickstrom M. 2001. Vertebrate pesticide toxicology manual (poisons). Information on Arellano-Sota C. 1988. Biology, ecology, and control poisons used in New Zealand as vertebrate of the vampire bat. Rev Infect Dis 10:S615. pesticides. Department of Conservation Techni- Arkins AM, Winnington AP, Anderson S, Clout MN. cal Series No. 23. Department of Conservation, 1999. Diet and nectarivorous foraging behaviour Wellington, New Zealand, 122 pp. of the short-tailed bat (Mystacina tuberculata). Eason CT, Murphy EC, Wright GRG, Spurr EB. J Zool Soc London 247:183–187. 2002. Assessment of risks of brodifacoum to non- Barclay RMR, Harder LD. 2003. Life histories of target birds and mammals in New Zealand. bats: Life in the slow lane. In: Bat ecology, Kunz Ecotoxicology 11:35–48. TH, Fenton MB, editors. University of Chicago, Eisemann JD, Swift CE. 2006. Ecological and human Chicago, Illinois, pp. 209–253. health hazards from broadcast application of Beath A, Thorne J, Robertson AW. 2004. Evaluating 0.005% diphacinone rodenticide baits in native the attractiveness of pest-control baits and lures Hawaiian ecosystems. In: Proceedings of the to captive short-tailed bats, Mystacina tubercu- 22nd vertebrate pest conference. Vertebrate Pest lata. Department of Conservation Science In- Conference, Berkeley, California, 6–9 March, ternal Series 189. Department of Conservation, pp. 413–433. Wellington, New Zealand, 19 pp. Erickson WA, Urban DJ. 2004. Potential risks of nine Berny P. 2007. Pesticides and the intoxication of wild rodenticides to birds and nontarget mammals: A animals. J Vet Pharmacol Ther 30:93–100. comparative approach. US Environmental Pro- Buckle AP. 1994. Rodent control methods: Chemi- tection Agency, Office of Prevention, Pesticides cal. In: Rodent pests and their control, Buckle and Toxic Substances, Washington, DC, USA, AP, Smith RH, editors. CAB International, 225 pp. Wallingford, UK, pp. 127–160. Fisher P, Broome K. 2010. Diphacinone. A review of Bullard RW, Thompson RD. 1977. Efficacy and current knowledge. Pesticide Review Series, safety of the systemic method of vampire bat Department of Conservation, Research and control. Interciencia 2:149–152. Development Group, Hamilton, New Zealand, Clark DR Jr, LaVal RK, Swineford DM. 1978. 38 pp. Dieldrin-induced mortality in an endangered Fisher P, O’Connor C, Wright G, Eason C. 2003. species, the gray bat (Myotis grisescens). Science Persistence of four anticoagulant rodenticides in 199:1357–1359. the livers of laboratory rats. Department of Clark DR Jr, Bagley FM, Waynon Johnson W. 1988. Conservation Science Internal Series 139. De- Northern Alabama colonies of the endangered partment of Conservation, Wellington, New grey bat Myotis grisescens: Organochlorine Zealand, 19 pp. contamination and mortality. Biol Conserv Fisher P, Spurr EB, Ogilvie SC, Eason CT. 2007. 43:213–225. Bait consumption and residual concentrations of Craddock P. 2003. Aspects of the ecology of forest diphacinone in the Wellington tree weta (Hemi- invertebrates and the use of brodifacoum. deina crassidens) (Orthoptera: Anostomatidae). Unpublished PhD Thesis, School of Biological New Zeal J Ecol 31:104–110. Sciences, University of Auckland, Auckland, Fournier-Chambrillon C, Berny PJ, Coiffier O, New Zealand, 236 pp. Barbedienne P, Dasse B, Delas G, Galineau H, Daniel MJ. 1976. Feeding by the short-tailed bat Mazet A, Pouzenc P, Rosoux R. 2004. Evidence (Mystacina tuberculata) on fruit and possibly of secondary poisoning of free-ranging riparian nectar. New Zeal J Zool 3:391–398. mustelids by anticoagulant rodenticides in Daniel MJ. 1990. Greater short-tailed bat. In: The France: Implications for conservation of Euro- handbook of New Zealand mammals, King CM, pean mink (Mustela lutreola). J Wildl Dis 40:688. editor. Oxford University Press, Auckland, New Gillies C, Styche A, Bradfield P, Chalmers K, Leach Zealand, pp. 131–136. M, Murphy E, Ward-Smith T, Warne R. 2006. Department of Conservation. 2000. Use of second Diphacinone bait for ground control of rats on generation anticoagulants on public conservation mainland conservation land. Science for Con- lands. Department of Conservation, Northern servation 270. Department of Conservation, Regional Office, Hamilton, New Zealand, 4 pp. Wellington, New Zealand, 20 pp. Eason C, Spurr E. 1995. Review of the toxicity and Howald G, Donlan CJ, Galvan JP, Russell JC, Parkes impacts of brodifacoum on non-target wildlife in J, Samaniego A, Wang YW, Veitch D, Genovesi New Zealand. New Zeal J Zool 22:371–379. P, Pascal M, et al. 2007. Invasive rodent Eason C, Henderson R, Hix S, MacMorran D, Miller eradication on islands. Conserv Biol 21:1258– A, Murphy E, Ross J, Ogilvie S. 2010. Alterna- 1268. DENNIS AND GARTRELL—DIPHACINONE TOXICITY IN NEW ZEALAND SHORT-TAILED BATS 0

Innes J, Barker G. 1999. Ecological consequences of Pascal M, Siorat F, Lorvelec O, Ye´sou P, Simberloff toxin use for mammalian pest control in New D. 2005. A pleasing consequence of Norway rat Zealand—An overview. New Zeal J Ecol 23:111– eradication: Two shrew species recover. Divers 127. Distrib 11:193–198. Johnston JJ, Pitt WC, Sugihara RT, Eisemann JD, Pryde MA, O’Donnell CFJ, Barker RJ. 2005. Factors Primus TM, Holmes MJ, Crocker J, Hart A. influencing survival and long-term population 2005. Probabilistic risk assessment for snails, viability of New Zealand long-tailed bats (Cha- slugs, and endangered honeycreepers in dipha- linolobus tuberculatus): Implications for conser- cinone rodenticide baited areas on Hawaii, USA. vation. Biol Conserv 126:175–185. Environ Toxicol Chem 24:1557–1567. Rattner BA, Horak KE, Lazarus RS, Eisenreich KM, King CM, editor. 2005. The handbook of New Meteyer CU, Volker SF, Campton CM, Eise- Zealand mammals, 2nd Ed. Oxford University mann JD, Johnston JJ. 2012. Assessment of Press, Melbourne, Australia, 596 pp. toxicity and potential risk of the anticoagulant Klite P. 1965. Intestinal bacterial flora and transit rodenticide diphacinone using eastern screech- time of three Neotropical bat species. J Bacteriol owls (Megascops asio). Ecotoxicology 21:832– 90:375–379. 846. Lemus JA, Bravo C, Garcı´a-Montijano M, Palacı´nC, Riley SPD, Bromley C, Poppenga RH, Uzal FA, Ponce C, Magan˜ a M, Alonso JC. 2011. Side Whited L, Sauvajot RM. 2007. Anticoagulant effects of rodent control on non-target species: exposure and notoedric mange in bobcats and Rodenticides increase parasite and pathogen mountain lions in urban southern California. burden in great bustards. Sci Total Environ J Wildlife Manage 71:1874–1884. 409:4729–4734. Robinson MH, Twigg LE, Wheeler SH, Martin GR. Lloyd B, McQueen S. 2000. An assessment of the 2005. Effect of the anticoagulant, pindone, on probability of secondary poisoning of forest the breeding performance and survival of insectivores following an aerial 1080 possum merino sheep, Ovis aries. Comp Biochem control operation. New Zeal J Ecol 24:47–56. Phys B 140:465–473. Lloyd BD. 1994. Evaluating the potential hazard of Salmon TP, Whisson DA, Berentsen AR, Gorenzel aerial 1080 poison operations to short-tailed bat WP. 2007. Comparison of 0.005% and 0.01% populations. Conservation Science Advisory diphacinone and chlorophacinone baits for Notes No. 108. Department of Conservation, controlling California ground squirrels (Spermo- Wellington, New Zealand, 12 pp. philus beecheyi). Wildl Res 34:14–18. McIlroy JC. 1986. The sensitivity of Australian Sedgeley J, Anderson M. 2000. Capture and captive animals to 1080 poison IX. Comparisons be- maintenance of short-tailed bats on Whenua tween the major groups of animals, and the Hou and monitoring of wild bats during the potential danger non-target species face from kiore eradication programme, winter 1998. 1080 poisoning campaigns. Wildl Res 13:39–48. Department of Conservation, Invercargill, New Mendenhall V, Pank L. 1980. Secondary poisoning Zealand, 64 pp. of owls by anticoagulant rodenticides. Wildlife Soc B 8:311–315. Sherley G, Wakelin M, McCartney J. 1999. Forest O’Donnell C. 2008. Mystacina tuberculata.In: invertebrates found on baits used in pest International Union for Conservation of Nature mammal control and the impact of sodium (IUCN) 2012, The IUCN Red List of Threatened monofluoroacetate (‘‘1080’’) on their numbers Species. Version 2012.1. www.iucnredlist.org. at Ohakune, North Island, New Zealand. New Accessed September 2012. Zeal J Zool 26:279–302. O’Donnell CFJ, Christie JE, Hitchmough RA, Lloyd Spurr E, Drew K. 1999. Invertebrates feeding on B, Parsons S. 2010. The conservation status of baits used for vertebrate pest control in New New Zealand bats, 2009. New Zeal J Zool Zealand. New Zeal J Ecol 23:167–173. 37:297–311. Stone W, Okoniewski J, Stedelin J. 2003. Anticoag- O’Donnell CFJ, Edmonds H, Hoare JM. 2011. ulant rodenticides and raptors: Recent findings Survival of PIT-tagged lesser short-tailed bats from New York, 1998–2001. B Environ Contam (Mystacina tuberculata) through a pest control Tox 70:34–40. operation using the toxin pindone in bait Stone WB, Okoniewski JC, Stedelin JR. 1999. stations. New Zeal J Ecol 35:291–295. Poisoning of wildlife with anticoagulant roden- O’Shea TJ, Clark DR Jr. 2002. An overview of ticides in New York. J Wildl Dis 35:187. contaminants and bats, with special reference to Thompson RD, Mitchell GC, Burns RJ. 1972. insecticides and the Indiana bat. In: The Indiana Vampire bat control by systemic treatment of bat: Biology and management of an endangered livestock with an anticoagulant. Science 177:806– species, Kurta A, Kennedy J, editors. Bat Conser- 808. vation International, Austin, Texas, pp. 237– Towns DR, Broome KG. 2003. From small Maria to 253. massive Campbell: Forty years of rat eradica- 0 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 1, JANUARY 2015

tions from New Zealand islands. New Zeal J Zool 2008 (revised June 24, 2008). US Environmental 30:377–398. Protection Agency. Office of Prevention, Pesti- Vyas NB. 1999. Factors influencing estimation of cides and Toxic Substances, Washington, DC, pesticide-related wildlife mortality. Toxicol Ind 37 pp. Health 15:187–192. Witmer GW, Boyd F, Hillis-Starr Z. 2007b. The Vyas NB, Rattner BA. 2012. Critique on the use of successful eradication of introduced roof rats the standardized avian acute oral toxicity test (Rattus rattus) from Buck Island using diphaci- for first generation anticoagulant rodentiticdes. none, followed by an irruption of house mice Hum Ecol Risk Assess 18:1069–1077. (Mus musculus). Wildl Res 34:108–115. Witmer G, Eisemann JD, Howald G. 2007a. The use Worthy T. 1997. Quaternary fossil fauna of South of rodenticides for conservation efforts. USDA Canterbury, South Island, New Zealand. JRoy National Wildlife Research Center – Staff Soc New Zeal 27:67–162. Publications. Paper 780, Lincoln, Nebraska, 167 pp. US Environmental Protection Agency. 2008. Risk Submitted for publication 11 July 2013. mitigation decision for ten rodenticides May 28, Accepted 2 June 2014.

View publication stats