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John E. Elliott, Barnett A. Rattner, Richard F. Shore, Nico W Van Den Brink, Paying the Pipers: Mitigating the Impact of Anticoagulant Rodenticides on Predators and Scavengers, BioScience, Volume 66, Issue 5, 01 May 2016, Pages 401–407, https://doi.org/10.1093/biosci/biw028
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Abstract
Anticoagulant rodenticides, mainly second-generation forms, or SGARs, dominate the global market for rodent control. Introduced in the 1970s to counter genetic resistance in rodent populations to first-generation compounds such as warfarin, SGARs are extremely toxic and highly effective killers. However, their tendency to persist and accumulate in the body has led to the widespread contamination of terrestrial predators and scavengers. Commercial chemicals that are classified by regulators as persistent, bio-accumulative, and toxic (PBT) chemicals and that are widely used with potential environmental release, such as dichloro-diphenyl-trichloroethane (DDT) or polychlorinated biphenyls (PCBs), have been removed from commerce. However, despite consistently failing ecological risk assessments, SGARs remain in use because of the demand for effective rodent-control options and the lack of safe and humane alternatives. Although new risk-mitigation measures for rodenticides are now in effect in some countries, the contamination and poisoning of nontarget wildlife are expected to continue. Here, we suggest options to further attenuate this problem.
Humans have occupied a large proportion of the globe's biodiversity hotspots, and in the process, many native species have been displaced and replaced with those that can tolerate or adapt to urban or agricultural landscapes (McKinney 2002). Among the most human-adapted species are rodents, particularly rat (Rattus) and mouse (Mus) species, which have been cohabiting with humans since Neolithic times (Reperant et al. 2013). There is a long history of humans attempting to control commensal rodents and contain the associated risks to human health from rodent-borne diseases, the destruction of food stores, and damage to infrastructure and other property. Recent estimates of the global impact of rodent pests are as high as $50 billion annually (Eason et al. 2010). Although many creative techniques have been devised to suppress rodent populations, for the past 50 years, as with most pest control, chemical biocides, primarily anticoagulant compounds, have been the dominant option worldwide. Once typified by the “blood-thinning” drug and rat poison warfarin, this prototypic first-generation anticoagulant (FGAR) compound has increasingly been replaced by more toxic and persistent analogues, or second-generation anticoagulant rodenticides (SGARs). Although highly effective, these chemicals are not specific to rodent pest species. Each year, US poison centers receive reports of rodenticide exposure by humans, mainly children, and ingestion by companion pets numbering in the tens of thousands (EPA 2011), and human exposures have been documented in Europe (Berny et al. 2010). SGAR contamination and poisoning of nontarget wildlife, particularly scavenging and predatory species such as raptorial birds, foxes, and weasels, which also provide important ecosystem services—including the control of rodent populations—are increasing in degree and scale (Rattner et al. 2014). As the extent of the environmental impact of anticoagulant usage became increasingly apparent over the past decade, agencies in North America, Europe, and elsewhere have wrestled with the regulatory challenge of balancing the demand for pest-control products with mitigating the impacts on nontarget organisms.
Widespread use, widespread contamination
Food production, storage, or transport facilities almost anywhere in the world may be commonly ringed with bait stations containing primarily SGARs. Less obvious are those placed into sewers, waste disposal, and transport operations anywhere with human food or wastes. Many homeowners and apartment building managers regularly deploy rodenticide baits in a prophylactic manner (EPA 2011). Sales and use data are difficult to obtain because they are considered confidential business information, but estimates are in the hundreds of millions of dollars annually in the United States and European countries, for example (Rattner et al. 2014).
Compared with major plant-protection products that are commonly applied by tractor or aircraft over large areas in attempts to locate and kill pests, the actual quantity of rodenticide active ingredient used is minor because of the extreme acute toxicity, particularly of the SGARs, and the targeted nature of their deployment. Although there are some exceptions—such as the field application of loose baits into “artificial plowed galleries” in France to control water voles (Arvicola terrestris; Courdassier et al. 2012) and broadcast usage in New Zealand for invasive mammals (Blackie et al. 2014)—the major use of rodenticides is via bait stations. These are deployed to attract target species that then disperse after consuming the poison and can become the food of many avian and mammalian predators and scavengers (figure 1). Ironically, those predators are also the primary natural agents of control. Many predators will switch their diets and prey on rats and commensal birds, which often are the most common prey available in human-dominated landscapes (Shore et al. 2003, Riley et al. 2007, Hindmarch and Elliott 2014, 2015a, 2015b).
Since the first reports of anticoagulant residues in British raptors (Newton et al. 1990), SGARs have become contaminants of avian and mammalian predators and scavengers in jurisdictions worldwide (table 1), including national parks remote from intensive human activities (Gabriel et al. 2012). Many questions still remain, and further research is needed to quantify what proportion of exposed animals are acutely poisoned, the importance of sublethal effects such as increased clotting times, and whether there are any population-level impacts (Thomas et al. 2011, Coeurdassier et al. 2012, Jacquot et al. 2013, Rattner et al. 2014, Hindmarch and Elliott 2015a). The fact remains, however, that there are now relatively few anthropogenic chemicals, other than SGARs, that are widespread contaminants of top predators and are lethal toxicants. It is important to recognize that chemicals that are lethally toxic to breeding adult birds at ambient environmental exposure have had some of the greatest impacts on populations of long-lived “k-selected” top predators, moreso in many instances than more subtle reproductive toxicants. Classic examples include the cyclodiene insecticide dieldrin in British raptors (Newton 1990), lead from hunters’ projectiles in California condors (Finkelstein et al. 2012), and most spectacularly, the veterinary drug diclofenac in Asian vultures (Oaks et al. 2004). By comparison, persistent organic pollutants (POPS), such as brominated flame retardants and perfluorinated surfactants, have received much more attention from scientists and regulators, and some are now scheduled for listing under the Stockholm Convention of Persistent Organic Pollutants, primarily on the basis of their persistence and bioaccumulative traits and long-range transport in the environment (http://chm.pops.int/TheConvention/ThePOPs/TheNewPOPs/tabid/2511/Default.aspx). However, in contrast to SGARs, currently, there is sparse evidence for significant effects of environmentally relevant concentrations of those compounds on wildlife populations, including the top predators that accumulate the greatest concentrations (e.g., Henny et al. 2009, Cesh et al. 2010, Harris and Elliott 2011, Fair et al. 2013). SGARs are lethal toxicants that are regularly deployed in a manner to provide a direct pathway and impact on rare and valuable top predators (Thomas et al. 2011, Gabriel et al. 2012, Rattner et al. 2014).
Species . | Sample Sizea . | Location . | Percentage incidence . | Reference . |
---|---|---|---|---|
Various raptors | 265 | New York, United States | 49 | Stone et al. 2003 |
Various raptors | 30 | France | 73 | Lambert et al. 2007 |
Tawny owl | 172 | United Kingdom | 19 | Walker et al. 2008a |
Red kite | 23 | United Kingdom | 74 | Walker et al. 2008b |
Various owl species | 164 | Western Canada | 70 | Albert et al. 2010 |
Various raptor species | 161 | Massachusetts, United States | 86 | Murray et al. 2011 |
Various raptors | 96 | California, United States | 92 | Lima and Salmon 2010 |
Great horned owl | 125 | Canada | 65 | Thomas et al. 2011 |
Various raptors | 430 | Denmark | 84–100 | Christensen et al. 2012 |
Various species | 129 | Spain | 28 | Sánchez-Barbudo et al. 2012 |
Various species | 773 | Scotland | 47 | Hughes et al. 2013 |
Various species | 30 | Norway | 53 | Langford et al. 2013 |
Barn owl | 63 | United Kingdom | 87 | Walker et al. 2014 |
Various raptors | 104 | Canary Islands | 61 | Ruiz-Suárez et al. 2014 |
Species . | Sample Sizea . | Location . | Percentage incidence . | Reference . |
---|---|---|---|---|
Various raptors | 265 | New York, United States | 49 | Stone et al. 2003 |
Various raptors | 30 | France | 73 | Lambert et al. 2007 |
Tawny owl | 172 | United Kingdom | 19 | Walker et al. 2008a |
Red kite | 23 | United Kingdom | 74 | Walker et al. 2008b |
Various owl species | 164 | Western Canada | 70 | Albert et al. 2010 |
Various raptor species | 161 | Massachusetts, United States | 86 | Murray et al. 2011 |
Various raptors | 96 | California, United States | 92 | Lima and Salmon 2010 |
Great horned owl | 125 | Canada | 65 | Thomas et al. 2011 |
Various raptors | 430 | Denmark | 84–100 | Christensen et al. 2012 |
Various species | 129 | Spain | 28 | Sánchez-Barbudo et al. 2012 |
Various species | 773 | Scotland | 47 | Hughes et al. 2013 |
Various species | 30 | Norway | 53 | Langford et al. 2013 |
Barn owl | 63 | United Kingdom | 87 | Walker et al. 2014 |
Various raptors | 104 | Canary Islands | 61 | Ruiz-Suárez et al. 2014 |
Percentage of samples with liver residues of at least 1 SGAR.
Species . | Sample Sizea . | Location . | Percentage incidence . | Reference . |
---|---|---|---|---|
Various raptors | 265 | New York, United States | 49 | Stone et al. 2003 |
Various raptors | 30 | France | 73 | Lambert et al. 2007 |
Tawny owl | 172 | United Kingdom | 19 | Walker et al. 2008a |
Red kite | 23 | United Kingdom | 74 | Walker et al. 2008b |
Various owl species | 164 | Western Canada | 70 | Albert et al. 2010 |
Various raptor species | 161 | Massachusetts, United States | 86 | Murray et al. 2011 |
Various raptors | 96 | California, United States | 92 | Lima and Salmon 2010 |
Great horned owl | 125 | Canada | 65 | Thomas et al. 2011 |
Various raptors | 430 | Denmark | 84–100 | Christensen et al. 2012 |
Various species | 129 | Spain | 28 | Sánchez-Barbudo et al. 2012 |
Various species | 773 | Scotland | 47 | Hughes et al. 2013 |
Various species | 30 | Norway | 53 | Langford et al. 2013 |
Barn owl | 63 | United Kingdom | 87 | Walker et al. 2014 |
Various raptors | 104 | Canary Islands | 61 | Ruiz-Suárez et al. 2014 |
Species . | Sample Sizea . | Location . | Percentage incidence . | Reference . |
---|---|---|---|---|
Various raptors | 265 | New York, United States | 49 | Stone et al. 2003 |
Various raptors | 30 | France | 73 | Lambert et al. 2007 |
Tawny owl | 172 | United Kingdom | 19 | Walker et al. 2008a |
Red kite | 23 | United Kingdom | 74 | Walker et al. 2008b |
Various owl species | 164 | Western Canada | 70 | Albert et al. 2010 |
Various raptor species | 161 | Massachusetts, United States | 86 | Murray et al. 2011 |
Various raptors | 96 | California, United States | 92 | Lima and Salmon 2010 |
Great horned owl | 125 | Canada | 65 | Thomas et al. 2011 |
Various raptors | 430 | Denmark | 84–100 | Christensen et al. 2012 |
Various species | 129 | Spain | 28 | Sánchez-Barbudo et al. 2012 |
Various species | 773 | Scotland | 47 | Hughes et al. 2013 |
Various species | 30 | Norway | 53 | Langford et al. 2013 |
Barn owl | 63 | United Kingdom | 87 | Walker et al. 2014 |
Various raptors | 104 | Canary Islands | 61 | Ruiz-Suárez et al. 2014 |
Percentage of samples with liver residues of at least 1 SGAR.
Although wildlife managers are concerned about the impact of SGARs on nontarget wildlife, somewhat ironically, these chemicals, particularly brodifacoum, have been widely used across the globe in conservation efforts to remove introduced rodents from previously predator-free islands. Entrenched populations of invasive rodents, principally R. norvegicus, have eliminated endemic bird and mammal species from some islands and severely affected breeding seabirds on many others (Howald et al. 2007). On some islands, populations of other predators are limited, but on islands along the Pacific coast of Canada and the United States, bald eagles (Haliaeetus leucocephalus), for example, have been poisoned during rat-eradication efforts (Howald et al. 1999). Like pesticide regulators, wildlife managers have opted to accept the risks of local contamination and impact on nontarget wildlife because of the effectiveness of anticoagulants and their cost efficiency over other options. Until alternative and safer control rodenticides are developed, it seems likely that such conservation use of SGARs will continue (e.g., Blackie et al. 2014).
Pathways forward
New risk-mitigation measures for anticoagulant use are now in effect in Canada (www.hc-sc.gc.ca/cps-spc/pubs/pest/_fact-fiche/restriction-rodenticides/index-eng.php) and more recently in the United States after a lengthy litigation process with one manufacturer (www2.epa.gov/rodenticides/canceling-some-d-con-mouse-and-rat-control-products). Point-of-sale measures restrict household users to first-generation anticoagulants or other rodenticides with alternate modes of action, such as the neurotoxin bromethalin. Packages are now limited in size and bait formulated into rigid blocks and sold with or in a tamper-resistant bait station. SGARs will, however, continue to be registered federally in the United States and Canada for use in and near buildings, waste receptacles and fence lines in agricultural settings, by licensed applicators. Again, data are limited on commercial sales, but one Canadian jurisdiction reported steady or increasing sales of commercial SGAR products over the period 1995 to 2009 (Elliott et al. 2014). The more toxic compounds, brodifacoum and difethialone, are now confined to indoor usage, with only the less toxic and persistent SGAR, bromadiolone, permitted for outdoor application. Those measures should reduce exposure of nontargets to the highly toxic SGARs. However, although technically indoor use, the potential continues for the movement of brodifacoum, for example, consumed by rodents to the exterior of unsealed buildings in these exposed rodents, putting predators at risk (Elliott et al. 2014). There is, therefore, a need to continue to monitor AR exposure and risk in nontarget populations.
The US state of California has gone further than the federal initiative. In California, the SGARs brodifacoum, bromadiolone, difenacoum and difethialone have been designated as “restricted materials” and can only be obtained and applied by a certified pesticide applicator under permit from a county commissioner. Aboveground bait may be placed no more than 50 feet from a manmade structure unless there is a feature that harbors or attracts targeted pests (www.cdpr.ca.gov/docs/legbills/rulepkgs/13-002/13-002.htm). In addition, the California Food and Agriculture Code (Section 12978.7) now prohibits the use of these SGARs in state parks, wildlife refuges, and conservancies.
In the European Union (EU), SGARs are recognized as posing significant risk to birds and nontarget mammals but continue to be authorized for use as biocides to protect public health and, in some member states, as plant-protection products. Several risk-mitigation measures (RMMs) have been suggested and applied in some member states by their authorities that deliver marketing authorizations (Berny et al. 2014). Because RMMs are set by each individual member state, a single commercial product may have more than one set of RMMs attached to its marketing authorizations across Europe.
The step taken in North America to remove SGARs from the domestic retail market should primarily reduce risk to humans, particularly children, and companion pets (www2.epa.gov/rodenticides/canceling-some-d-con-mouse-and-rat-control-products). Cross-border e-commerce may provide a loophole to gain access to restricted pesticides, including rodenticides in some jurisdictions. However, in the United States, for example, online sales of pesticides have been subject to the same controls as purchases from traditional stores for more than a decade (EPA 2004). The exposure of nontarget wildlife to SGAR products should also decrease in suburban and urban areas, where domestic use is a major contributor. However, nontargets, particularly predators and scavengers, may continue to encounter substantial residues certainly of bromadiolone and potentially of the more toxic SGARs in their diet from continuing use in structural and food production and transport facilities.
The development of safe and effective rodenticides is a complex research and development challenge, although there are some promising new advances (Blackie et al. 2014). Until such time, we suggest a three-pronged approach that could further mitigate adverse nontarget effects.
Rationalize usage and deployment strategies
The first of these, which is already being implemented by some corporations and jurisdictions, is to rationalize usage and deployment strategies. For decades, structural rodent management relied on the regular, prophylactic use of rodenticides to prevent infestations and meet health and safety standards. Bait stations were required to be placed at specified intervals and were subject to audit. The focus was on the placement of bait rather than on testing efficacy in rodent control. Recently, in the United States, however, under the EPA's Pesticide Environmental Stewardship Program (PESP), some major food and “big-box” retailers have moved to greatly reduce rodenticide usage in their food-supply chains (www.epa.gov/pestwise/pesp/members/strategies/walmart.pdf). That approach essentially employs the long-established principles of integrated pest management (IPM) to monitor pest presence and apply pesticides only as needed. It also takes the concept further to develop, for example, “Go Green” programs which have used data on the ecology and behavior of rodents to develop more effective control programs.
A cautionary note, however: Although there are data on cost savings to corporate and other end users from such IPM-based reductions in usage (Arjo et al. 2009), it is much less clear whether changing from prophylactic to evidence-driven bait deployment has resulted in significant reductions in the availability of poisoned rodents to predators and scavengers. There is some evidence that restrictions on the field use of anticoagulants in France resulted in both decreased amounts of products applied and increased population densities of the red fox (Vulpes vulpes) following periods of reduced rodenticide usage (Jacquot et al. 2013). We are not aware of other studies that quantified the mitigating efficiency on actual risks. For other types of pesticide application, such quantification was essential to ensure the implementation of mitigating measures, such as the effectiveness of buffer zones and the use of specific spray nozzles to minimize the spray drift of pesticides into adjacent waterbodies (e.g., de Snoo and de Wit 1998). That has resulted in sophisticated models to assess spray drifts and is implemented in the guidance of pesticide use and its further regulation and labeling (Hewitt 2000). Without such quantitative evidence, the justification for specific IPM measures may encounter skepticism and opposition from some stakeholders.
Develop and implement outreach and educational stewardship programs
The second measure would be consideration for the further development and implementation of outreach and educational stewardship programs by industry and government. Such programs are already in effect in areas of Europe (www.cefic.org/Documents/About-Us/Industry%20sectors/EBPF/Guideline-on-Best-Practice-in-the-Use-of-Rodenticides-in-the-EU.pdf), and arguably the most developed is the stewardship scheme commencing in the United Kingdom in 2016 (www.thinkwildlife.org/stewardship-regime). That has been developed and led by an industry consortium (www.thinkwildlife.org/about-crru) working with the relevant Competent Authority and has the overall aim of reducing exposure in nontarget wildlife while ensuring efficacious rodent control, including areas where there is resistance to some SGARs. The program, underpinned by the development and dissemination of a code of best practice (www.thinkwildlife.org/crru-downloads/crru-uk-code-of-best-practice), involves multiple activities, including approval and certification of training courses and a requirement of proof of competence at the point of sale of professional products. A further major component is the monitoring of outcomes, with data assessed by the Competent Authority. Such monitoring includes the periodic survey of the knowledge, attitudes, and practices of all professional rodenticide users; the independent monitoring of changes in exposure (as measured from tissue residues) in a sentinel nontarget species, the barn owl Tyto alba (Shore et al. 2014); and the evaluation of the breeding success of selected barn owl populations in relation to rodenticide use. Top predators, such as the barn owl, provide broad ecosystem services, including the regulation of rodent populations.
Implementing a paying-the-piper strategy
A third measure might entail compensation for the collateral damage of predatory birds and mammals and could be considered, although the analogy is not perfect, as a paying-the-piper approach. The cost of impact on rodent-regulating allies, including raptors, weasels, canines, and felids, could be borne generally by users of the products, not the commons (viz. imposition of a form of the polluter-pays principle). The concept is widely recognized and is simply that those who damage or deplete the environment should bear the costs. Applications of the concept include having resource extractors pay for not only the costs of waste disposal, cleanup, and restoration but also the costs of enforcing the regulations. That is effectively a form of paying for ecosystem services (Engel et al. 2008). Other examples include the payment of deposit fees on beverage containers, as well as ecofees on car batteries, tires, and other products (Driedger 2001). Many agree that the principle is inherently sound and logical, both “legally and economically” (OECD 2008); differences surround defining who or what is affected by the pollution and, therefore, who should be compensated (Driesen 1997). Some of the arguments about the principle are fundamentally rooted in differences in political philosophy, related to views on private property rights and the contention that owners of private property and therefore resources make better stewards (and therefore conservationists) than the commons or public (Cordato 2001). In the majority of political jurisdictions, however, the reality is a mix of public and private ownership of land and resources, and wild plants and animals are considered to be public resources and the property of the state or commons (Geist et al. 2001).
There are already farsighted examples in which the polluter-pays approach in the form of fees, levies, or responsibility for education and monitoring of impacts have been applied to management and regulation of rodenticides. California set a precedent by implementing an eco-fee system at point of sale (www.vpcrac.org/about/surcharge-legislation), whereby a fee of $ 0.50 per pound (227.5 grams) is added to the cost of vertebrate-pest-control products (e.g., anticoagulant rodenticides). Fees are used mainly for research on the development of alternative products, improvements in the safe use of existing products, and investigation of toxicity and environmental effects. It also should be recognized that, as we discussed above, in the United Kingdom, SGAR manufacturers and suppliers aim to pay what can be considered effectively a fixed eco-fee by developing, leading, and funding a comprehensive SGAR stewardship program.
We suggest that the broader application of such a paying-the-piper approach, in concert with the rationalized deployment and educational outreach, could help offset the impact of the ongoing global use of SGAR compounds. Fees might be used more broadly, such as for compensation and mitigation programs for the affected predators, in the form of active management of both populations and habitat. There are precedents for the use of money in this way obtained in the United States from Natural Resource Damage Assessments of oils spills and contaminated sites (www.epa.gov/superfund/programs/nrd/primer.htm). The most recent and well-publicized example is the settlement between the US federal government and BP to compensate for injury and damage to resources resulting from the Deep Water Horizon oil spill (www.doi.gov/deepwaterhorizon).
Conclusions
Given the likelihood that anticoagulant rodenticides will continue to be deployed widely across the globe to suppress pest rodent populations, then some ongoing impacts on nontarget wildlife seem inevitable. Here, we suggest that in addition to recent risk-mitigation measures that have been imposed in some jurisdictions, other activities might be implemented. Namely, we suggest that (a) industry consider the implementation of validated IPM procedures to reduce and optimize use of products, (b) user groups adopt effective education and outreach programs for applicators and the public, and (c) the consideration of eco-fees on rodenticide sales, similar to those in effect in California (www.vpcrac.org/about/surcharge-legislation). Such fees could be used to raise funds for research into developing new products, investigating and monitoring select nontarget species, and providing compensation for habitat or mitigation measures for affected nontarget populations. Given that governments elsewhere in the world rely heavily on the United States and Europe for leadership in chemical regulations, the adoption of these proposed measures could have broader implications.
S. Lee assisted with the artwork. C. Bishop reviewed earlier versions of the manuscript. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.
References cited