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Anticoagulant Rodenticides: Implications for Wildlife Rehabilitation

  • 360 Environmental
Anticoagulant Rodenticides: Implications for Wildlife Rehabilitation
Author: Michael T. Lohr
Affiliation: School of Science, Edith Cowan University, Joondalup, Western Australia 6027,
Email address:
Anticoagulant rodenticides (ARs) are commonly used to control rodents worldwide for the
purposes of reducing disease transmission, agricultural losses, and damage to homes and
property (Bradbury, 2008). In the 1970s and 1980s “second generation anticoagulant
rodenticides (SGARs) were developed to overcome resistance which had developed in some
rodent species. SGARs are more acutely toxic and have half-lives which are substantially
longer than first generation anticoagulant rodenticides (FGARs) (Thomas et al., 2011). As a
consequence, SGARs are much more likely to bioaccumulate and biomagnify, leading to a
substantially higher risk of secondary toxicity in non-target wildlife. Cases of apparently
poisoned wildlife being brought to wildlife rehabilitation centres have already been
documented (Grillo et al., 2016). Sub-lethal AR exposure may also increase the likelihood of
wildlife entering care by increasing the probability of collisions with vehicles and
anthropogenic structures (Albert et al., 2010; Mendenhall and Pank, 1980; Newton et al.,
1990; Stone et al., 2003) and susceptibility to parasitism (Lemus et al., 2011; Riley et al.,
2007; Serieys et al., 2018). Emerging evidence indicates that secondary AR toxicity is an
important threatening process impacting wildlife across Australia (Lohr and Davis, 2018).
The tendency of SGARs to biomagnify increases the likelihood of impacts on scavengers and
carnivores in higher trophic levels. Species with long lifespans and low reproductive rates are
more likely to suffer population-level impacts from AR toxicity (Rattner et al., 2014).
Effective rehabilitation may be especially important in these instances.
Challenges in Treating Poisoned Wildlife
A number of challenges exist in treating wildlife exposed to ARs. Susceptibility to ARs
varies dramatically both between and within species (Thomas et al., 2011). Treatment of AR
poisoning in wildlife with an unknown history of exposure can be substantially more
complicated than treatment of companion animals and humans where the type and quantity of
the poison are often known. Unlike companion animals and humans, wildlife exposed
through secondary poisoning are frequently exposed to multiple rodenticides (Christensen et
al., 2012; Hughes et al., 2013; Murray, 2017; Walker et al., 2011). Little is known about
effects of exposure to multiple ARs but some research suggests that the interactions between
ARs may be synergistic rather than simply additive (Mosterd and Thijssen, 1991). Treatment
is further complicated by a lack of species-specific guidelines for treating AR toxicity. The
necessity of managing rodents within wildlife rehabilitation facilities can present additional
challenges for wildlife rehabilitators. Understanding general principles relating to how ARs
function may aid in successful diagnosis and treatment of poisoned individuals and help
reduce the likelihood of unintentional poisoning during necessary rodent control activities.
ARs function by blocking the recycling of vitamin K in the liver. Vitamin K is required in the
synthesis of several important blood clotting factors. Onset of symptoms is usually delayed
for several days after ingestion of ARs because it takes several days to exhaust the body’s
reserves of vitamin K once recycling has been blocked. Symptoms of AR toxicity in wildlife
can include: anaemia, intramuscular or subcutaneous haemorrhage in the absence of physical
trauma, pale mucous membranes, difficulty breathing (due to blood in the lungs), reduced
activity, anorexia, bleeding from the mouth or nares, and blood in stool or droppings
(Murray, 2017). Unfortunately, confirmation of the specific ARs involved in suspected
poisonings can be difficult because ARs are only detectable in blood for a short period of
time relative to other tissues (Erickson and Urban, 2004). As a consequence, negative test
results can be misleading and should not be taken as an indication that poisoning has not
occurred. Concentrations of ARs in plasma also do not correlate with the duration of
treatment required in poisoned animals (Gunja et al., 2011). Accurate confirmation of the
type and concentration of ARs involved in the poisoning requires analysis of liver tissue and
is not appropriate for diagnosis of living animals.
Toward a Treatment Protocol
In humans and companion animals, prothrombin time and other measurements of clotting
times are typically used in the diagnosis of AR toxicity (Rattner et al., 2014). Clotting times
which are more than 25% longer than baseline values for the relevant species suggest
potential AR poisoning and are likely to be useful in evaluating wildlife with suspected AR
exposure (Rattner et al., 2014). While no formal treatment protocols appear to be available
specifically for wildlife exposed to ARs, a treatment regime used successfully in dogs
diagnosed with AR poisoning involved an initial oral administration of 5 mg/kg of vitamin K1
split into two or three doses throughout the day (Robben et al., 1998). Vitamin K
administration was repeated daily at this dosage until the condition of the animal stabilised
and prothrombin time returned to normal (Robben et al., 1998). Daily dosage of vitamin K1
was then reduced by between 30% and 50% on each subsequent day unless prothrombin time
increased (Robben et al., 1998). Treatment was ceased when prothrombin times did not
increase after two to four days without vitamin K1 supplementation. Duration of treatment in
this study lasted for up to 30 days (Robben et al., 1998) but treatment of some human cases of
SGAR poisoning has required up to six months of treatment (Gunja et al., 2011). Necessary
treatment durations for exposed wildlife are likely to vary substantially dependant on
exposure levels, type of ARs involved, individual genetic factors, and susceptibility of the
species involved. It is also important to keep in mind that due to long persistence time in liver
tissue, SGARs will still be present and partially blocking vitamin K recycling even after
prothrombin times and associated blood clotting return to normal levels. Animals with
residual SGARs in their livers will be vulnerable to future exposure at lower doses relative to
animals with no ARs accumulated in liver tissue. At present, no practical solution to this
problem exists.
Managing Rodents at Wildlife Care Centres
Facilities engaged in the rehabilitation of wildlife face additional practical difficulties in
managing rodents, due, in part, to the availability of spilled or uneaten food provided to
animals in care. In most wildlife rehabilitation facilities, commensal rodents present an
unacceptable risk of disease transmission, infrastructure damage, and predation of smaller
species in care. However, in several instances, raptors in rehabilitation facilities have been
lethally poisoned with ARs as a consequence of poisoned rodents entering their enclosures
(Mooney, 2017). Careful consideration needs to be given to the management of rodent pests
within wildlife rehabilitation facilities to ensure the safety of animals in care.
In some instances, rodent abundance and associated negative outcomes can be sufficiently
reduced through non-lethal means. When practical, reduction of rodent food sources by
prompt removal of uneaten food provided to injured wildlife, use of feeders which prevent
spillage, and picking up fallen fruits in landscaped areas can aid in reducing rodent numbers.
Sealing holes and other potential entry points in buildings and enclosures can also reduce
rodent access to food resources while simultaneously excluding them from areas where they
are likely to cause damage. Reducing available rodent habitat by cleaning up brush piles and
rubbish can aid in reducing activity and abundance of commensal rodents. Replacing dense
introduced vegetation especially palms with native plants reduces rodent nesting habitat
and provides better habitat for native avian predators which help control rodents.
Lethal control methods can also be helpful in reducing rodent numbers once the factors
driving rodent abundance have been addressed to the degree practicable. A wide variety of
lethal traps are readily available for control of commensal rodents. Careful positioning of the
traps is necessary to ensure efficacy at capturing rodents and reduce harm to non-target
species. These considerations will vary dramatically with trap design. If rodenticides are
used, baits containing the FGARs warfarin and coumatetralyl are substantially less likely to
cause secondary toxicity than SGARs, due to their relatively short half-life and lower toxicity
(Erickson and Urban, 2004). However, resistance to FGARs may reduce their utility in rodent
control in some areas. The distribution and prevalence of resistance to FGARs among
commensal rodent species in Australia is poorly known but has been documented in Sydney
as early as 1978 (Saunders, 1978). If resistance is suspected, baits containing the active
ingredient cholocalciferol may be helpful. Cholecalciferol is not an anticoagulant and is
effective at controlling rodents which have developed resistance to ARs. It is also
substantially less likely than SGARs to cause secondary poisoning in native wildlife but does
carry a limited risk of secondary toxicity which likely varies by species (Eason et al., 2000).
While many obstacles to effective treatment of AR toxicity in Australian wildlife exist at
present, several factors may help to reduce the incidence and severity of such events and
improve treatment outcomes in the future. The Australian Pesticides and Veterinary
Medicines Authority is currently reviewing the scheduling of SGARs (Australian Pesticides
and Veterinary Medicines Authority, 2015) and recommendations suggesting more stringent
regulation of SGARs have been published (Lohr and Davis, 2018). Ongoing research into the
ecology of AR exposure may also improve future treatment protocols. Future work assessing
exposure rates and sensitivity to ARs across a wide variety of Australian wildlife species will
be contribute substantially to our knowledge of the probability of AR exposure and allow
more rapid assessment of animals admitted to rehabilitation centres. Research into patterns in
spatial distribution of AR exposure will also allow faster identification of individuals at high
risk of poisoning and potentially improve treatment outcomes.
Albert, C.A., Wilson, L.K., Mineau, P., Trudeau, S., Elliott, J.E., 2010. Anticoagulant
rodenticides in three owl species from Western Canada, 1988-2003. Arch. Environ.
Contam. Toxicol. 58, 451459.
Australian Pesticides and Veterinary Medicines Authority, 2015. Second generation anti-
coagulant rodenticidespriority 2 [WWW Document]. URL (accessed 7.14.17).
Bradbury, S., 2008. Risk Mitigation Decision for Ten Rodenticides. Washington D. C., USA.
Christensen, T.K., Lassen, P., Elmeros, M., 2012. High Exposure Rates of Anticoagulant
Rodenticides in Predatory Bird Species in Intensively Managed Landscapes in Denmark.
Arch. Environ. Contam. Toxicol. 63, 437444.
Eason, C.T., Wickstrom, M., Henderson, R., Milne, L., Arthur, D., 2000. Non-target and
Secondary Poisoning Risks Associated with Cholecalciferol, in: Proceedings of the New
Zealand Plant Protection Conference. New Zealand Plant Protection Society, pp. 299304.
Erickson, W., Urban, D., 2004. Potential Risk of Nine Rodenticides to Birds and Mammals:
A Comparative Approach. Washington DC.
Grillo, T., Cox-Witton, K., Gilchrist, S., Ban, S., 2016. Suspected rodenticide poisoning in
possums. Anim. Heal. Surveill. Q. 21, 8.
Gunja, N., Coggins, A., Bidny, S., 2011. Management of intentional superwarfarin poisoning
with long-term vitamin K and brodifacoum levels. Clin. Toxicol. 49, 385390.
Hughes, J., Sharp, E., Taylor, M.J., Melton, L., Hartley, G., 2013. Monitoring agricultural
rodenticide use and secondary exposure of raptors in Scotland. Ecotoxicology 22, 974
Lemus, J.A., Bravo, C., García-Montijano, M., Palacín, C., Ponce, C., Magaña, M., Alonso,
J.C., 2011. Side effects of rodent control on non-target species: Rodenticides increase
parasite and pathogen burden in great bustards. Sci. Total Environ. 409, 47294734.
Lohr, M.T., Davis, R.A., 2018. Anticoagulant rodenticide use , non-target impacts and
regulation: A case study from Australia. Sci. Total Environ. 634, 13721384.
Mendenhall, V.M., Pank, L.F., 1980. Secondary Poisoning of Owls by Anticoagulant
Rodenticides. Wildl. Soc. Bull. 8, 311315.
Mooney, N., 2017. Risks of Anticoagulant Rodenticides to Tasmanian Raptors. Tasmanian
Bird Rep. 38, 1725.
Mosterd, J.J., Thijssen, H.H.W., 1991. The long-term effects of the rodenticide, brodifacoum,
on blood coagulation and vitamin K metabolism in rats. Br. J. Pharmacol. 104, 531535.
Murray, M., 2017. Anticoagulant rodenticide exposure and toxicosis in four species of birds
of prey in Massachusetts, USA, 2012 2016, in relation to use of rodenticides by pest
management professionals. Ecotoxicology 26, 10411050.
Newton, I., Wyllie, I., Freestone, P., 1990. Rodenticides in British barn owls. Environ. Pollut.
68, 101117.
Rattner, B.A., Lazarus, R.S., Elliott, J.E., Shore, R.F., van den Brink, N., 2014. Adverse
Outcome Pathway and Risks of Anticoagulant Rodenticides to Predatory Wildlife.
Environ. Sci. Technol. 48, 84338445.
Riley, S.P.D., Bromley, C., Poppenga, R.H., Uzal, F.A., Whited, L., Sauvajot, R.M., 2007.
Anticoagulant Exposure and Notoedric Mange in Bobcats and Mountain Lions in Urban
Southern California. J. Wildl. Manage. 71, 18741884.
Robben, J.H., Kuijpers, E.A.P., Mout, H.C.A., 1998. Plasma superwarfarin levels and vitamin
K1 treatment in dogs with anticoagulant rodenticide poisoning. Vet. Q. 20, 2427.
Saunders, G.R., 1978. Resistance to Warfarin in the Roof Rat in Sydney, NSW. Search 9, 39
Serieys, L.E.K., Lea, A.J., Epeldegui, M., Armenta, T.C., Moriarty, J., VandeWoude, S.,
Carver, S., Foley, J., Wayne, R.K., Riley, S.P.D., Uittenbogaart, C.H., 2018. Urbanization
and anticoagulant poisons promote immune dysfunction in bobcats. Proc. R. Soc. B
Biol. Sci. 285, 20172533.
Stone, W.B., Okoniewski, J.C., Stedelin, J.R., 2003. Anticoagulant rodenticides and raptors:
Recent findings from New York, 1998-2001. Bull. Environ. Contam. Toxicol. 70, 3440.
Thomas, P.J., Mineau, P., Shore, R.F., Champoux, L., Martin, P. a., Wilson, L.K., Fitzgerald,
G., Elliott, J.E., 2011. Second generation anticoagulant rodenticides in predatory birds:
Probabilistic characterisation of toxic liver concentrations and implications for predatory
bird populations in Canada. Environ. Int. 37, 914920.
Walker, L.A., Chaplow, J.S., Llewellyn, N.R., Pereira, M.G., Potter, E.D., Sainsbury, A.W.,
Shore, R.F., 2011. Anticoagulant rodenticides in predatory birds 2011: a Predatory Bird
Monitoring Scheme (PBMS) report. Lancaster, UK.
ResearchGate has not been able to resolve any citations for this publication.
Full-text available
The impacts of anticoagulant rodenticides (ARs) on non-target wildlife have been well documented in Europe and North America. While these studies are informative, patterns of non-target poisoning of wildlife elsewhere in the world may differ substantially from patterns occurring in Australia and other countries outside of cool temperate regions due to differences in the types of ARs used, patterns of use, legislation governing sales, and potential pathways of secondary exposure. Most of these differences suggest that the extent and severity of AR poisoning in wildlife may be greater in Australia than elsewhere in the world. While many anecdotal accounts of rodenticide toxicity were found-especially in conjunction with government control efforts and island eradications-no published studies have directly tested rodenticide exposure in non-target Australian wildlife in a comprehensive manner. The effects of private and agricultural use of rodenticides on wildlife have not been adequately assessed. Synthesis of reviewed literature suggests that anticoagulant rodenticides may pose previously unrecognised threats to wildlife and indigenous people in Australia and other nations with diverse and abundant reptile faunas relative to countries with cooler climates where most rodenticide ecotoxicology studies have been conducted. To address the identified knowledge gaps we suggest additional research into the role of reptiles as potential AR vectors, potential novel routes of human exposure, and comprehensive monitoring of rodenticide exposure in Australian wildlife, especially threatened and endangered omnivores and carnivores. Additionally, we recommend regulatory action to harmonise Australian management of ARs with existing and developing global norms.
Full-text available
Understanding how human activities influence immune response to environmental stressors can support biodiversity conservation across increasingly urbanizing landscapes. We studied a bobcat (Lynx rufus) population in urban southern California that experienced a rapid population decline from 2002-2005 due to notoedric mange. Because anticoagulant rodenticide (AR) exposure was an underlying complication in mange deaths, we aimed to understand sublethal contributions of urbanization and ARs on 65 biochemical markers of immune and organ function. Variance in immunological variables was primarily associated with AR exposure and secondarily with urbanization. Use of urban habitat and AR exposure has pervasive, complex and predictable effects on biochemical markers of immune and organ function in free-ranging bobcats that include impacts on neutrophil, lymphocyte and cytokine populations, total bilirubin and phosphorus. We find evidence of both inflammatory response and immune suppression associated with urban land use and rat poison exposure that could influence susceptibility to opportunistic infections. Consequently, AR exposure may influence mortality and has population-level effects, as previous work in the focal population has revealed substantial mortality caused by mange infection. The secondary effects of anticoagulant exposure may be a worldwide, largely unrecognized problem affecting a variety of vertebrate species in human-dominated environments.
Full-text available
Restrictions on second-generation anticoagulant rodenticides (SGARs) in the United States, which were partially implemented in 2011, prohibit the sale of SGAR products through general consumer outlets to minimize use by non-professional or non-agricultural applicators. This study analyzed liver tissue from four species of birds of prey admitted to a wildlife clinic in Massachusetts, USA, from 2012-2016 for residues of anticoagulant rodenticides (ARs). Ninety-four birds were analyzed; 16 were symptomatic for AR toxicosis, and 78 asymptomatic. Ninety-six percent of all birds tested were positive for SGARs: 100% of those diagnosed with AR toxicosis ante-mortem and/or post-mortem and 95% of subclinically exposed birds. Brodifacoum was found in 95% of all birds. Sixty-six percent of all birds contained residues of two or more SGARs. A significant increase in exposures to multiple SGARs occurred in later years in the study. Pesticide use reports (PURs) filed with the Massachusetts Department of Agricultural Resources were reviewed to determine the frequency of use of different ARs by pest management professionals (PMPs) across five years. This study finds that the three SGARs favored by PMPs-bromadiolone, difethialone, brodifacoum-were present in combination in the majority of birds, with increases in multiple exposures driven by increased detections of bromadiolone and difethialone. Continued monitoring of AR residues in nontarget species following full implementation of sales and packaging restrictions in the US is needed in order to elucidate the role of PMP use of SGARs in wildlife exposures and to evaluate the effectiveness of current mitigation measures.
Full-text available
In New Zealand cholecalciferol-containing baits are used for possum and rodent control. We have assessed the primary and secondary non- target hazards associated with these baits. At 2000 mg/kg cholecalciferol had no adverse effects in ducks, but some chickens and canaries died. Weta and weka were not affected by eating bait containing cholecalciferol. In secondary poisoning studies most dogs and cats fed carcasses of possums poisoned with cholecalciferol were unaffected, but repeat exposures for 5 days induced some reversible signs of toxicosis in dogs. The most distinguishing feature of cholecalciferol is a lower risk of secondary poisoning when compared with 1080 and brodifacoum.
Full-text available
Despite the documented risk of secondary poisoning to non-target species by anticoagulant rodenticides there is no statutory post-approval monitoring of their use in the UK. This paper presents results from two Scottish monitoring schemes for the period 2000-2010; recording rodenticide use on arable farms and the presence of residues in raptor carcasses. More than three quarters of arable farms used anticoagulant rodenticides; predominately the second generation compounds difenacoum and bromadiolone. There was widespread exposure to anticoagulant rodenticides in liver tissues of the raptor species tested and the residues encountered generally reflected agricultural use patterns. As found in other studies, Red Kites (Milvus milvus) appeared to be particularly vulnerable to rodenticide exposure, 70 % of those sampled (n = 114) contained residues and 10 % died as a result of rodenticide ingestion. More unexpectedly, sparrowhawks (Accipiter nisus), which prey almost exclusively on birds, had similar exposure rates to species which prey on rodents. Although, with the exception of kites, confirmed mortality from rodenticides was low, the widespread exposure recorded is concerning. Particularly when coupled with a lack of data about the sub-lethal effects of these compounds. This raises questions regarding whether statutory monitoring of use is needed; both to address whether there are deficiencies in compliance with approval conditions or whether the recommended risk management procedures are themselves adequate to protect non-target wildlife.
Anticoagulants - compounds that prevent clotting of the blood - are extensively used for control of small mammal pests. The potential secondary hazards of 6 anticoagulant rodenticides to birds of prey were examined in this study. Whole rats or mice were killed with each anticoagulant and were fed to 1-3 species of owls. Owls died of hemorrhaging after feeding on rats killed with bromadiolone, brodifacoum, or diphacinone; sublethal hemorrhaging occurred in owls fed rats killed with difenacoum. These results demonstrate potential secondary hazards of 4 anticoagulants to avian predators. No abnormalities were observed in owls fed rats killed with fumarin and chlorophacinone.
Despite a long history of successful use, routine application of some anticoagulant rodenticides (ARs) may be at a crossroad due to new regulatory guidelines intended to mitigate risk. An adverse outcome pathway for ARs was developed to identify information gaps and endpoints to assess the effectiveness of regulations. This framework describes chemical properties of ARs, established macromolecular interactions by inhibition of vitamin K epoxide reductase, cellular responses including altered clotting factor processing and coagulopathy, organ level effects such as hemorrhage, organism responses with linkages to reduced fitness and mortality, and potential consequences to predator populations. Risk assessments have led to restrictions affecting use of some second-generation ARs (SGARs) in North America. While the European regulatory community highlighted significant or unacceptable risk of ARs to non-target wildlife, use of SGARs in most EU member states remains authorized due to public health concerns and the absence of safe alternatives. For purposes of conservation and restoration of island habitats, SGARs remain a mainstay for eradication of invasive species. There are significant data gaps related to exposure pathways, comparative species sensitivity, consequences of sublethal effects, potential hazards of greater AR residues in genetically-resistant prey, effects of low-level exposure to multiple rodenticides, and quantitative data on the magnitude of non-target wildlife mortality.
Humans introduce many toxicants into the environment, the long-term and indirect effects of which are generally unknown. We investigated exposure to anticoagulant rodenticides and evaluated the association between notoedric mange, an ectoparasitic disease, and anticoagulant exposure in bobcats (Lynx rufus) and mountain lions (Puma concolor) in a fragmented urban landscape in southern California, USA. Beginning in 2002, an epizootic of notoedric mange, a disease previously reported only as isolated cases in wild felids, in 2 years reduced the annual survival rate of bobcats from 0.77 (5-yr average) to 0.28. Anticoagulants were present in 35 of 39 (90%) bobcats we tested, multiple compounds were present in 27 of these 35 (77%), and total toxicant load was positively associated with the use of developed areas by radiocollared animals. Mange-associated mortality in bobcats showed a strong association with anticoagulant exposure, as 19 of 19 (100%) bobcats that died with severe mange were also exposed to the toxicants, and for bobcats with anticoagulant residues >0.05 ppm, the association with mange was highly significant (X2 = 10.36, P = 0.001). We speculate that concomitant elevated levels of rodenticide exposure may have increased the susceptibility of bobcats to advanced mange disease. Bobcats were locally extirpated from some isolated habitat patches and have been slow to recover. In 2004, 2 adult mountain lions died directly from anticoagulant toxicity, and both animals also had infestations of notoedric mange, although not as advanced as in the emaciated bobcats that died with severe disease. Two other mountain lions that died in intraspecific fights also exhibited exposure to 2-4 different anticoagulants. These results show that the effects of secondary poisoning on predators can be widespread, reach even the highest-level carnivores, and have both direct and possibly indirect effects on mortality. Further research is needed to investigate the lethal and sub-lethal effects of anticoagulants and other toxicants on wildlife in terrestrial environments.