Article

Kinetics of bromadiolone in rodent populations and implications for predators after field control of the water vole, Arvicola terrestris

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Abstract

We document the kinetics of bromadiolone in two rodent populations after a field control of water voles, and their implications for predator exposure. Water voles and common voles were trapped aboveground and underground from 1 to 135 days after bromadiolone treatment in the field. Livers, digestive tracts, and rests of the body were analyzed separately. Our results indicate that 99.6% of the water voles trapped underground and 41% of the common voles trapped aboveground contain bromadiolone residues. Concentrations were maximal between 3.3 and 6.5 days after treatment, according to the tissues examined and the model applied for water voles, and after 1.3 to 3.7 days for common voles. Water voles appeared available almost exclusively for foraging predators. Common voles, found less likely to be poisoned and exhibiting weaker concentrations, were mainly sampled aboveground. The liver, primarily eaten by some predators and scavengers, contains a larger bromadiolone quantity (59% of the total amount found in water voles). The rejection of the digestive tract by those species may lead to a subsequent consumption of voles with higher bromadiolone concentrations (from +3.8 to +5.8% of concentration) and provide a moderate risk increase. After 135 days, eight of the ten water voles and one of the two common voles exhibited detectable residues. Additionally, one specimen presented higher concentrations than the others, and similar to those measured in Voles trapped between the first 15-20 days. This may have consequences on predator intoxications several months after treatment. These results integrate individual differences for the two main rodent species present in treated areas. Implications for predator exposure were investigated at the end of the study and suggest that, if the risk of secondary poisoning is maximal during the first 15-20 days when the rodent densities remain high, exposure conditions are maintained for at least 135 days.

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... Since the 1970s, most of population control strategies aimed to reduce the spread of fossorial water voles involve rodenticides, frequently bromadiolone (Defaut et al. 2009). High persistence of this rodenticide in the field allows voles to continue feeding beyond the lethal dose (Sage et al. 2008), and toxic bait can remain in store chamber inside burrows, being available for survivors and colonizers for long periods . Thus, large proportion of contaminated fossorial water voles can be available for predators . ...
... Thus, large proportion of contaminated fossorial water voles can be available for predators . Most A. scherman specimens remain in their galleries when they fall ill, being only available for predators such as mustelids and foxes (Sage et al. 2008), but 38 % of them can die aboveground (Saucy et al. 2001) and hence be consumed by birds of prey or scavengers, such as crows, buzzards or owls (Sage et al. 2008;Montaz et al. 2014 (Defaut et al. 2009). High grazing intensity, the removal of the protective grass cover or soil cultivation cause the destruction of vegetation shelter which in turn promotes predation pressure and dehydration (Morilhat et al. 2007 and references therein;Defaut et al. 2009). ...
... Thus, large proportion of contaminated fossorial water voles can be available for predators . Most A. scherman specimens remain in their galleries when they fall ill, being only available for predators such as mustelids and foxes (Sage et al. 2008), but 38 % of them can die aboveground (Saucy et al. 2001) and hence be consumed by birds of prey or scavengers, such as crows, buzzards or owls (Sage et al. 2008;Montaz et al. 2014 (Defaut et al. 2009). High grazing intensity, the removal of the protective grass cover or soil cultivation cause the destruction of vegetation shelter which in turn promotes predation pressure and dehydration (Morilhat et al. 2007 and references therein;Defaut et al. 2009). ...
Thesis
The montane water vole Arvicola scherman occurs in mountainous areas of Europe, living in underground burrow systems located in grasslands and fruit orchards. This species feeds on the root system of plants, including fruit trees. Specifically, the subspecies A. scherman cantabriae is nowadays one of the main causes of economical loss in apple orchards of Asturias (northwestern Spain). An official control program in Spain considers all sustainable phytosanitary measures that can reduce population growth of this species. Since the pest condition of A. scherman depends on its biology and ecology, a deep knowledge of these aspects is needed to set up specific and suitable control strategies. Thus, the aim of this research is to obtain essential information on the reproductive biology and population genetics of this species in the agricultural landscape of Asturias. More than 800 individuals of A. scherman cantabriae were gathered in apple orchards located at low altitude in Villaviciosa and Nava municipalities during two annual cycles (from February 2011 to January 2013). Sexual characteristics, body measurements and relative age class of each specimen were recorded. Body condition of females, which indicates energy provision, and the number of embryos of each one were also wrote down. Skeletal muscle samples of 137 specimens from ten demes were used to conduct a microsatellite-based analysis (12 microsatellite loci). These orchards are placed in a landscape conformed by a mosaic of small and different land-use plots, which was assessed in a vector based geographic information system and it was focused on soil-occupancy categories. Pregnant females and young specimens were detected over the whole year, which mean that A. scherman cantabriae showed a continuous breeding pattern during the study period. Intra-annual changes in body mass and size of sexual organs of males did not affect significantly reproduction at a population scale. Thus, primary demands of these voles seem to be properly fulfilled during the whole year and hence energy budgets can be destined to cop continuous reproduction. To our knowledge, no other A. scherman population shows regularly this reproductive pattern. Females were able to produce a high number of litters per year (7.30) although litter size was relatively moderate (embryos/female: first year: 3.87; second year: 3.63). Each female was able to produce 28.25 pups per year. The reproductive potential showed by Cantabrian voles is, to our knowledge, the highest one reported to date for this species; probably because the breeding season does not entail a critical factor in this area. A positive correlation between litter size and the body condition of the mother was observed. Therefore, the body condition of females seems to be one of the main factors involved in the variation of the reproductive potential in A. scherman cantabriae. These studied demes showed relatively low level of genetic diversity (HE = 0.621; HO = 0.601; AR = 4.42) probably due to both the inbreeding and genetic drift effects. Significant genetic differentiation appeared among demes, which revealed a strong pattern of significant isolation-by-distance both for Euclidean distances (r = 0.790) and effective distances (r = 0.780). The spatial autocorrelation analysis detected four genetic clusters or populations in this study area (120 km2). Thus, this mosaic of different land-use plots decreases connectivity among suitable habitats even at local scale, in which A. scherman populations mainly depend on birth and death rates. An estuary and a four-lane road did not suppose a barrier for gene flow of this species. Less seasonal environment and highly patched landscape would suggest that this species does not show well marked multiannual fluctuations of density at large scale in this area. Control strategies for A. scherman cantabriae at a regional scale can be discarded. The monitoring of each population, or management unit, will be essential to know the population dynamic and to establish coordinated control strategies. Preserving and promoting this patchy landscape would favour the presence of predators and hamper dispersion of this species. A continuous population control throughout the year would be advisable, using sustainable methods, such as traps, the installation of barriers and/or coordinated manipulation of habitat.
... Trapping was conducted by members of the FREDON Franche-Comté at a different untreated commune within the region during a WV outbreak. We used Topcat kill traps (Topcat GmbH, Wintersingen, Switzerland) 38 and stored the dead WVs at −20 ∘ C until the day of tunnel setting (i.e. placement of the cap and wooden board). ...
... 8,45 We also collected two common voles (hereafter CVs) from T. Site 4 and five CVs at U. Site 4. CVs may also consume the bromadiolone bait and are also prey of SMs, thus they are an additional route of bromadiolone trophic transfer for SMs. 46,47 After collection, the voles were frozen at −20 ∘ C. 38 In the laboratory, we dissected them and sampled 0.5 g of liver tissue for AR analyses. 44 Vole livers and scat subsamples were stored at −20 ∘ C until analysis. ...
... Site 4, 35-days parcel) where bromadiolone was used, as one of the two bromadiolone-positive WV livers collected there contained bromadiolone residue at 0.015 mg kg −1 (though the concentration can reach 6 mg kg −1 in the 20 days immediately after treatment). 12,38 In addition, two CVs were also positive for bromadiolone there, containing up to 0.285 mg kg −1 . Within the treated sites, there were high probabilities that SMs foraged in the treated parcels and were in contact with poisoned rodents (8-54% of the farming surface was treated during 2016 at the treated sites). ...
Article
BACKGROUND The use of pesticides can affect non‐target species by causing population declines through indirect intoxication. Small mustelids (SMs; weasels, Mustela nivalis L.; stoats, Mustela erminea L.) consume water voles (WVs, Arvicola scherman S.) and can be exposed to bromadiolone, an anticoagulant rodenticide used in some countries to reduce WV damage to grasslands. Here, we investigated whether bromadiolone affected SM abundance. RESULTS We monitored SM abundance using footprint tracking tunnels in spring and autumn at 10 sites. Among these sites, 4 were treated with bromadiolone, while 6 were not treated. We found reduced SM abundance at these 4 sites from spring to autumn (treated sites, mean±SE SM abundance change=‐1.68±0.42; untreated sites, 0.29±0.25). Using a linear model, we observed that SM abundance decreased as a function of the quantity of bromadiolone applied during the 3 months before the autumn estimate. We found that WV abundance increased at treated sites (linear model, treated sites, mean±SE WV abundance change=1.4±0.4; untreated sites, 0.33±0.25). Thus, at treated sites, SM abundance declined despite increased food availability. By analyzing residues in vole livers and SM scats we showed that SMs may be exposed to bromadiolone at the sites where this compound was used. CONCLUSION This study is the first to document the relationship between SM abundance and bromadiolone usage for small mammal control. Declines in SM abundance were observed at treated sites, where bromadiolone residue was found in SM scats. This correlative approach suggests that bromadiolone treatment may lead to seasonal SM declines and associated WV increases. This article is protected by copyright. All rights reserved.
... The disrupted behaviour of intoxicated rodents may make them easy prey for predators (Cox and Smith, 1992). Bromadiolone may persist in voles for at least 4 months after treatments, though in lower concentrations than during the immediate weeks after treatment, given the metabolization and excretion of bromadiolone (Sage et al., 2008). There is evidence of secondary exposure to bromadiolone in the common weasel in northern and central Europe (Elmeros et al., 2011;Fernandez-de-Simon et al., 2019;Koivisto et al., 2018;McDonald et al., 1998), but it is unreported if weasels in southwestern Europe are also exposed. ...
... We also registered the general condition of the animal in different body parts, searching for instance for skin bruises, state of organs and lymph nodes, etc. We collected the liver, which is the main organ of storage of bromadiolone in vertebrates (Sage et al., 2008;Sánchez-Barbudo et al., 2012). The liver was then wrapped in aluminum foil and immediately frozen at −20°C (Fernandez-de-Simon et al., 2019). ...
... However, it is known that ARs have been also used illegally at least in one study area (Villalar de los Comuneros, Valladolid) during years with no vole pest, to control bird species (Martínez-Padilla et al., 2017), and this illegal and uncontrolled use could also explain part of our results (see below). For the variable of elapsed time since the last known bromadiolone treatment, we grouped the information into three levels: (i) 0-6 months after bromadiolone application, when exposure and probabilities of weasels eating voles with high bromadiolone load is eventually possible (Sage et al., 2008), (ii) 6-12 months, when exposure is still possible, but levels of bromadiolone concentration in vole prey are expected to be low (Sage et al., 2008), and (iii) >12 months, when there is the lowest risk of exposure, given the short life expectancy of common voles and other small mammals (usually <1 year in natural conditions; IUCN, 2016). We use these long periods because our data are estimates and the application time of bromadiolone baits can be long (i.e., applications might not have happened right after the bait was provided to farmers (Junta de Castilla y León, 2016). ...
Article
Bromadiolone is an anticoagulant rodenticide (AR) commonly used as a plant protection product (PPP) against rodent pests in agricultural lands. ARs can be transferred trophically to predators/scavengers when they consume intoxicated live or dead rodents. ARs exposure in weasels Mustela nivalis, small mustelids specialized on rodent predation, is poorly known in southern Europe. Moreover, in this species there is no information on bioaccumulation of AR diastereomers e.g., cis- and trans-bromadiolone. Trans-bromadiolone is more persistent in the rodent liver and thus, is expected to have a greater probability of trophic transfer to predators. Here, we report on bromadiolone occurrence, total concentrations and diastereomers proportions (trans- and cis-bromadiolone) in weasels from Castilla y León (north-western Spain) collected in 2010–2017, where bromadiolone was irregularly applied to control outbreaks of common voles Microtus arvalis mainly with cereal grain bait distributed by the regional government. We also tested variables possibly associated with bromadiolone occurrence and concentration, such as individual features (e.g., sex), spatio-temporal variables (e.g., year), and exposure risk (e.g., vole outbreaks). Overall bromadiolone occurrence in weasels was 22% (n = 32, arithmetic mean of concentration of bromadiolone positives = 0.072 mg/kg). An individual showed signs of bromadiolone intoxication (i.e., evidence of macroscopic hemorrhages or hyperaemia and hepatic bromadiolone concentration > 0.1 mg/kg). All the exposed weasels (n = 7) showed only trans-bromadiolone diastereomer in liver, whilst a single analyzed bait from those applied in Castilla y León contained trans- and cis-bromadiolone at 65/35%. Bromadiolone occurrence and concentration in weasels varied yearly. Occurrence was higher in 2012 (100% of weasels), when bromadiolone was widely distributed, compared to 2016–2017 (2016: 20%; 2017: 8.33%) when bromadiolone was exceptionally permitted. The highest concentrations happened in 2014 and 2017, both years with vole outbreaks. Our findings indicate that specialist rodent predators could be exposed to bromadiolone in areas and periods with bromadiolone treatments against vole outbreaks.
... Furthermore, use of ARs to protect croplands, grassland and forestry also self-evidently requires open area deployment of rodenticides. When used outdoors, baits can be placed down the burrow entrance of the target species (Khan et al. 1998;Tobin et al. 1997) or specifically inserted into tunnel/gallery systems (Jacquot et al. 2013;Sage et al. 2008). This may to some extent reduce but not eliminate non-target exposure but efficacy of control of target species will in part depend on ability to locate a high proportion of occupied burrows. ...
... Compared with wood mice and bank voles, fewer non-target Microtus voles were exposed when ARs were used as biocides (median: 7%; range 3-19.5%), although common voles were widely exposed (36-41% of individuals contaminated) when ARs were used as plant protection products against the sympatric water vole (Jacquot et al. 2013;Sage et al. 2008). Shrews were also frequently exposed to ARs in the studies we examined. ...
... It may be possible to estimate TBCs from AR liver residues for SGARs as liver burdens have been shown to be good predictors of total body burden for bromadiolone in voles (Winters et al. 2010). Liver:TBC ratios have been reported in Microtus species (6.0, 8.8, and 5.2) and water vole (4.9) for bromadiolone (Giraudoux et al. 2006;Sage et al. 2008;Winters et al. 2010) and in poisoned laboratory mice (4.8) for brodifacoum (Newton et al. 1990). The median value of those five ratios (5.2) can be used to estimate TBCs in live-trapped animals for which liver residues were measured (Table 6.2). ...
Chapter
The toxicity of anticoagulant rodenticides to non-target species is one of the root concerns over wide-scale use of these compounds. Compared with the numerous studies documenting secondary exposure in predators, there have been relatively few studies on primary exposure in non-targets. We consider why primary exposure of non-targets occurs, which species are most likely to be exposed, how and why exposure magnitude varies, and whether exposure results in ecologically significant effects. Species groups or trophic guilds most at risk of primary exposure include invertebrates, reptiles, birds and mammals. Relatively little is known about exposure and particularly effects in invertebrates and reptiles although recent studies suggest that anticoagulants may impact invertebrates, presumably through different toxic pathways to those that result in vertebrate toxicity. Amongst higher vertebrates, primary exposure occurs in some bird species but there is little information on extent and importance. There are more studies on non-target mammals and it is granivorous species that are most likely to feed on bait and accumulate residues, as might be predicted given their ecological and trophic similarities to target species. However, studies suggest a surprisingly high degree of exposure in shrews, although it is unclear the extent to which this is primary and/or secondary. Overall, arguably the most striking aspect of primary exposure in mammals is the large-scale variation both in the proportion of animals exposed and the magnitude of residues accumulated. We consider the multiple abiotic and biotic factors that may drive this, including the direct and indirect effects of resistance in target species. In terms of ecologically significant effects, primary exposure clearly does cause acute mortalities in non-target vertebrates and these have been associated with significant population impacts on intensively baited islands where there has been limited or no potential for immigration. Localised population impacts have also been documented in mainland small mammals but most non-targets are likely to be r-selected species. Population declines may therefore be expected to be relatively short-term, provided baiting is episodic, as population numbers can recover through high intrinsic rate of reproduction in survivors, reduced density-dependent mortality, and immigration. However, prolonged or permanent baiting may potentially result in long-term depletion of resident non-target populations that is ameliorated only by immigration; such areas may act as population sinks.
... To date, the field works interested in ARs transfer to wildlife have focused mainly on living rodents (Brakes and Smith 2005;Giraudoux et al. 2006;Sage et al. 2008;Winters et al. 2010). It was notably shown that the residues measured in rodents trapped alive may lead to daily doses higher than LD50 (the median lethal dose) determined for different predators (Coeurdassier et al. 2012;Giraudoux et al. 2006;Tosh et al. 2011). ...
... In a study that aimed at assessing how exposure of Brandt voles Microtus brandti to bromadiolone varied over time, Winters et al. (2010) found 11 carcasses of Brandt voles in the 8 days following field application of bromadiolone baits. In field trials achieved in France, less than 4 % of the water vole populations were found dead aboveground despite a daily survey of the plot during 10 days after the treatment (Demoly et al. 1999cited in Saucy et al. 2001Sage et al. 2008). However, in an experiment in which scavenging was prevented, it was demonstrated that 30 % of water voles died aboveground after a treatment with bromadiolone (Saucy et al. 2001). ...
... Moreover, bromadiolone residues were 6 times higher in the carcasses of Brandt voles dead aboveground than in the body of those trapped alive (Winters et al. 2010). In the only dead water vole found aboveground, Sage et al. (2008) reported a concentration of 3.1 mg of bromadiolone/kg of whole body, which was among the highest measured in the population sampled. Thus, after treatments, carcasses with high residues burdens of AR available aboveground could represent one of the main routes of exposure for wildlife during control operations of rodents. ...
Article
Full-text available
Worldwide, agricultural uses of anticoagulant rodenticides (ARs) cause poisonings of non-target wildlife as observed in France where bromadiolone is used to control water vole outbreaks. Following bromadiolone field application, a part of the vole population may die aboveground of the treated plots and thus, can represent an important risk of secondary poisoning for scavengers. In this study, water voles were trapped in a non-treated area and their carcasses were placed aboveground in plots located in an area where a vole outbreak occurred. Then, the environmental persistence, the diurnal and nocturnal scavenging rates of water vole carcasses were assessed in autumn 2011 and in spring 2012. The diurnal scavenger species were also identified. The environmental persistence of the carcasses to reach at least a scavenging rate of 87.5 % was 0.5-1.5 day. The average rates of diurnal and nocturnal scavenging ranged from 67 to 100 % and 5 to 100 %, respectively. They depended on the composition of the scavenger community present near the monitored plots; diurnal scavenging rates being higher with corvids than with raptors. In autumn, the red kite and the common buzzard were the main scavengers in one of the plots, what suggests a high risk of poisoning for these raptors during post-nuptial migration. So, the collection of vole carcasses after treatments and the limitations of bromadiolone applications when high densities of predators/scavengers are observed could be implemented to mitigate the risks of secondary poisoning.
... Up to 60 000 ha were treated in Franche-Comté (eastern France) in 1998 when outbreaks occurred. Application is via wheat baits coated with bromadiolone which are delivered in ploughed artificial galleries to treated fields and then eaten by voles (Sage et al. 2007(Sage et al. , 2008. The treatments are primarily applied in autumn (from September to December) and in spring (April and May). ...
... The Red Kite is an opportunistic predator and scavenger that may exhibit local diet specialization in time and space according to prey availability (Cramp & Simmons 1980, Carter 2001. Therefore, during Water Vole outbreaks, it is likely that Red Kites feed largely on this species, which accumulates high residues of bromadiolone following treatment and thus represents a high risk of exposure for this raptor (Sage et al. 2008). The diet of Red Kites has been studied in different contexts (Cramp & Simmons 1980), including during a Common Vole outbreak in Spain (Sunyer & Viñuela 1994, Garcia et al. 1998; however, to our knowledge, no data are available on the diet of Red Kites during Water Vole outbreaks. ...
... This paper aims to document the diet of Red Kites during a Water Vole outbreak in eastern France by analysing macro-remains in regurgitated pellets collected during autumn 2008. Based on data on bromadiolone residues in Voles following treatment (Sage et al. 2008), the results are used to assess the ecotoxicological risk of secondary poi-soning to Red Kites under different exposure scenarios. ...
Article
Poisoning by pesticides is considered one of the primary threats to the Red Kite Milvus milvus. We studied the diet of this raptor in an area of eastern France where the rodenticide bromadiolone is widely used to control Water Vole Arvicola terrestris outbreaks. A high degree of specialization for Water Voles was noted, as their remains were identified in all 119 pellets collected in autumn 2008, whereas other small rodent species and insects occurred in 27 and 9% of pellets, respectively. We estimated that Water Voles constituted 94% of the total biomass ingested by Red Kites under these conditions. Based on these data, the risk of secondary poisoning due to feeding on poisoned voles was assessed. Acute exposure on a single day was not considered a risk for Kites, but exposure to poisoned voles over 1 week represented the maximal risk for the Red Kite; the calculated dose of bromadiolone ingested by a Red Kite was 137 times higher than the toxicological benchmark for birds. A field survey in the studied area detected four dead Red Kites and one moribund bird in autumn 2008 but did not confirm that the cause of death was bromadiolone poisoning. We suggest that professional monitoring is needed to assess the impact of rodenticides on Red Kites in areas where voles are controlled.
... Rodenticide positive non-target Apodemus mice, common vole (Microtus arvalis), and bank voles have been recorded up to 750 m from farms with chemical rodent control (Tosh et al. 2012;Coeurdassier et al. 2018). Caching of bait or long distance dispersal of rodents may explain the minute levels of BRM found in a bank vole near one of the study sites prior to the experimental application of poison (Szacki 1999;Sage et al. 2008;Stradiotto et al. 2009;Coeurdassier et al. 2018). ...
... We analysed the total body concentrations in the small nontarget mammals. Up to 20% of the total quantity of bromadiolone quantity in voles is found in the digestive track (Sage et al. 2008). Diet analyses based on undigested contend in the stomach-intestine tract from mammalian predators show that they regularly eat the whole mice or vole (e.g. ...
... Madsen et al. 2002;Hammershøj et al. 2004;Elmeros 2006;Elmeros et al. 2008). Contrary, avian predators often discard the digestive tract of small mammal prey when feeding (Sage et al. 2008 and reference therein). Thus, raptors would receive a lower dose per prey individual than the total body BRM levels determined in the present study would indicate. ...
Article
Full-text available
The extensive use of anticoagulant rodenticides (ARs) results in widespread unintentional exposure of non-target rodents and secondary poisoning of predators despite regulatory measures to manage and reduce exposure risk. To elucidate on the potential vectoring of ARs into surrounding habitats by non-target small mammals, we determined bromadiolone prevalence and concentrations in rodents and shrews near bait boxes during an experimental application of the poison for 2 weeks. Overall, bromadiolone was detected in 12.6% of all small rodents and insectivores. Less than 20 m from bait boxes, 48.6% of small mammals had detectable levels of bromadiolone. The prevalence of poisoned small mammals decreased with distance to bait boxes, but bromadiolone concentration in the rodenticide positive individuals did not. Poisoned small mammals were trapped up to 89 m from bait boxes. Bromadiolone concentrations in yellow-necked mice (Apodemus flavicollis) were higher than concentrations in bank vole (Myodes glareolus), field vole (Microtus agrestis), harvest mouse (Micromys minutus), and common shrew (Sorex araneus). Our field trials documents that chemical rodent control results in widespread exposure of non-target small mammals and that AR poisoned small mammals disperse away from bating sites to become available to predators and scavengers in large areas of the landscape. The results suggest that the unintentional secondary exposure of predators and scavengers is an unavoidable consequence of chemical rodent control outside buildings and infrastructures.
... At the time of this study, the authors were unaware of the work of Atterby et al. (2005) and Sage et al. (2008) who analyzed entire brown rat (Rattus norvegicus) and water vole (Arvicola terrestris) carcasses to determine anticoagulant body burdens. Because we could not sufficiently dissolve vole pelts, heads, and paws for reliable bromadiolone analysis, these tissues were excluded from the analysis. ...
... Total average total bromadiolone residues (2.65 70.53 mg/kg and 13.7073.82) in voles exposed to 50 and 500 mg/kg bromadiolone baits during this study were much lower than those reported by Sage et al. (2008;196.5 mg/kg). Giraudoux et al. (2006) also reported a higher maximum concentration of bromadiolone in a vole exposed to 50 mg/kg baits than those observed in a vole exposed 500 mg/kg baits during this study (30.23 mg/kg compared to 24.37 mg/kg, respectively). ...
... In our study, the greatest amount of bromadiolone in exposed voles was sequestered in their livers (61.4% of the total burden, when both measured and estimated body amounts are included in the calculation). These data are consistent with those of Sage et al. (2008) who found 59% of sequestered bromadiolone in the livers of water voles. However, Giraudoux et al. (2006) reported a lower accumulation (25%) in livers of water voles. ...
Article
In 2002, hundreds of non-target wildlife deaths occurred in Mongolia following aerial applications of bromadiolone, an anticoagulant rodenticide, to control eruptive Brandt's vole (Microtus brandti) populations. To clarify whether secondary poisoning could have contributed to these deaths, a field study was undertaken in Mongolia to measure bromadiolone residues in voles following exposure to two concentrations (50 and 500 mg/kg) of bromadiolone-treated wheat. The two treatments produced different total burdens (2.65 microg+/-0.53SE and 13.70 microg+/-3.82SE, respectively) and liver burdens (1.74 microg+/-0.33SE and 8.81 microg+/-2.33SE, respectively) of bromadiolone in voles (both p<0.05). Total burdens of bromadiolone in voles found dead above ground were higher than those of live-trapped voles (32.35 microg+/-17.98SE versus 5.18 microg+/-1.40SE, respectively; p<0.05). These results are valuable for future assessments of secondary poisoning risk to scavengers and predators from large-scale bromadiolone poisoning operations of the type undertaken in Mongolia.
... By late July of that year, an extensive control campaign was in place which affected circa 500,000 ha. Rodenticides represent a significant risk for non-target species such as granivores, and their predators (Berny et al., 1997;Shore et al., 2003;Sage et al., 2008;Sarabia et al., 2008;Walker et al., 2008;Olea et al., 2009). Moreover, the storage of rodenticide baits by voles in cavities increases the persistence of the rodenticide in the environment, which increases the risk of secondary poisoning in predator species (Sage et al., 2007). ...
... CP concentrations in some voles found dead were actually relatively low, which suggests that in voles at least, this toxicant was effective even at quite low doses. If this could be confirmed experimentally with captive voles, such results may permit a reduction in the CP dose used in bait, and thus potentially mitigate unwanted and important effects upon non-target species (Sage et al., 2008;Olea et al., 2009). Moreover, since CP was found to be effective in killing voles, this may indicate that the large scale use of more persistent 2nd generation rodenticides (which carry a higher risk of secondary poisoning for scavengers) may be unneces-sary (Berny et al., 1997;Walker et al., 2008;Sage et al., 2008). ...
... If this could be confirmed experimentally with captive voles, such results may permit a reduction in the CP dose used in bait, and thus potentially mitigate unwanted and important effects upon non-target species (Sage et al., 2008;Olea et al., 2009). Moreover, since CP was found to be effective in killing voles, this may indicate that the large scale use of more persistent 2nd generation rodenticides (which carry a higher risk of secondary poisoning for scavengers) may be unneces-sary (Berny et al., 1997;Walker et al., 2008;Sage et al., 2008). Some voles with CP residues in liver did not show signs of hemorrhage (33%), as was the case with pigeons (23.5%) found dead within the same study area (Sarabia et al., 2008). ...
Article
Full-text available
A common vole (Microtus arvalis) population peak in Northern Spain in 2007 was treated with large scale application of chlorophacinone, an anticoagulant rodenticide of the indandione family. Voles found dead and trapped alive were collected in treated and untreated areas. Residues of chlorophacinone were analyzed in liver of voles by HPLC-UV. Also, the presence of the pathogen Francisella tularensis was analyzed by PCR in samples of vole spleen. Chlorophacinone (82-3800 ng/g; wet weight liver) was only detected in voles found dead in treated areas (55.5%). The prevalence of F. tularensis in voles found dead in treated areas was also particularly high (66.7%). Moreover, chlorophacinone levels were lower in voles that were PCR-positive for F. tularensis (geometric mean [95% CI], 418 [143-1219] ng/g) than in those that were PCR-negative (1084 [581-2121] ng/g). Interactions between pathogens and rodenticides might be considered to reduce the doses used in baits or to avoid the use of the more toxic 2nd generation anticoagulant rodenticides.
... Brodifacoum (43.5%) and bromadiolone (32%) were detected most often in liver tissue. This is not surprising because these compounds are used most frequently in Germany and this result confirms other findings (Berny et al., 1997;Sage et al., 2008). Little is known about what habitat features are related to AR exposure in red foxes. ...
... 32% der Proben nachgewiesen wurden. Damit kamen die am häufigsten verwendeten AR Wirkstoffe Brodifacoum und Bromadiolon auch am häufigsten vor und das Vorkommen von AR Rückständen lag in diesen Rotfüchsen in einem Bereich, der auch in anderen Studien gefunden wurde(Berny et al., 1997;Sage et al., 2008). Wenig ist darüber bekannt, welche Habitate die Exposition von Rotfüchsen und anderen Prädatoren gegenüber AR begünstigen. ...
... Individuen Rückstände mehrerer Wirkstoffe trugen. Durch die weite Verbreitung dieser Art, die Nutzung unterschiedlichster Lebensräume, das opportunistische Verhalten bei der Nahrungssuche(Börner, 2014;Contesse et al., 2004;Meisner et al., 2014) sowie die hohe Expositionswahrscheinlichkeit gegenüber verschiedenen AR(Berny et al., 1997;Sage et al., 2008; scheint dieses Raubtier für das Monitoring und den Vergleich von AR-Expositionen zwischen ländlichen und urbanen Räumen besonders geeignet zu sein(López-Perea et al., 2019). Ein wichtiger Parameter für die Beurteilung von AR-Expositionsszenarien ist dabei neben der Siedlungsfläche auch die Bevölkerungsdichte(López-Perea et al., 2015). ...
Technical Report
Full-text available
Zur Regulierung von Schadnagerpopulationen werden im Biozidbereich in Deutschland in den meisten Fällen Fraßköder mit blutgerinnungshemmenden (antikoagulanten) Wirkstoffen eingesetzt. Antikoagulante Rodentizide wirken bei allen warmblütigen Tieren, also auch bei Organismen, die nicht bekämpft werden sollen oder dürfen. Zudem sind die meisten dieser Wirkstoffe persistent, bioakkumulierend und toxisch. Um Nichtzielorganismen zu schützen und Einträge in die Umwelt zu minimieren, wurden bei der Biozid-Zulassung von antikoagulanten Rodentiziden verbindliche Risikominderungsmaßnahmen festgeschrieben. Die Effektivität dieser Maßnahmen ist jedoch kaum empirisch untersucht, so dass Wissensdefizite auch im Hinblick auf eine mögliche Optimierung bzw. Weiterentwicklung von Risikominderungsmaßnahmen bestehen. Im Rahmen dieses Forschungs- und Entwicklungsvorhabens wurden daher drei zentrale Aspekte mit Bezug auf den Schutz von Nichtzielorganismen näher betrachtet. Im ersten Teil wurde untersucht, wie sich die Ausbringung antikoagulanter Rodentizide in Köderstationen ausschließlich innerhalb von Gebäuden im Vergleich zum Einsatz in und um Gebäude auf das Auftreten blutgerinnungshemmender Wirkstoffe in freilebenden Nichtzielkleinsäugern auswirkt. Weiterhin wurden die Bewegungsmuster und Sterbeorte vergifteter Wanderratten auf Bauernhöfen dokumentiert, um daraus Rückschlüsse auf die mögliche Exposition von Beutegreifern ziehen zu können. Im zweiten Teil wurden Rückstände antikoagulanter Rodentizide in Rotfüchsen aus ländlichen und urbanen Räumen untersucht, um mögliche Unterschiede in der Exposition zu identifizieren. Außerdem wurde das Auftreten blutgerinnungshemmender Wirkstoffe in verschiedenen Singvögeln während Rattenbekämpfungen auf landwirtschaftlichen Betrieben analysiert. Im dritten Teil wurde versucht, die Ausbringung von Fraßködern in Köderstationen so zu gestalten, dass Nichtzielorganismen von der Köderannahme ausgeschlossen werden. *** In Germany, in most cases anticoagulant rodenticides are used to control commensal pest rodents in the biocide sector. These agents are effective not only in target species but also in other vertebrate taxa. Moreover, most anticoagulants are persistent, bioaccumulative and toxic. In order to mitigate risk and to minimise release into the environment, mandatory risk mitigation measures were stipulated within the biocidal products authorisation. However, their efficiency has not yet been empirically tested and information for advancing risk mitigation measures is missing. In this research and development project, we focused on three aspects of risk mitigation measures with regard to the protection of non-target species. Firstly, we investigated whether applying anticoagulant rodenticides in bait stations exclusively inside buildings has an effect on the occurrence and concentration of anticoagulant residues in non-target small mammals com- pared to their application in and around buildings. Additionally, we observed spatio-temporal patterns of poisoned Norway rats on farms and we documented the locations where poisoned individuals succumbed to rodenticides. Secondly, anticoagulant residues in red foxes from rural and urban regions were analysed to identify possible differences in exposure. Furthermore, the occurrence of anticoagulant residues in different songbird species during rat control on farms was investigated. Thirdly, we developed and tested a new bait station design that aimed to exclude non-target small mammals from bait consumption.
... While some species that depend on agro-ecosystems are declining (Aviron et al., 2009), others are outbreaking according to specific time laps and are considered as agricultural pests Koyanagi et al., 2012;Krebs, 2013). Small mammal pests, including some grassland voles (e.g. the montane water vole (Arvicola scherman) and the common vole (Microtus arvalis)), have been widely studied with concern about agricultural economy, ecotoxicology, eco-epidemiology and fundamental ecology (Parshad, 1999;Hanski et al., 2001;Zhang et al., 2003;Korpimäki et al., 2004;Giraudoux et al., 2006;Sage et al., 2008;Sluydts et al., 2009;Wang et al., 2010;Decors et al., 2011;Fraschina et al., 2012;Gabriel et al., 2012). ...
... Localisation d'exemples de pullulations de micro-mammifères dans le monde.Ces « pestes agricoles » ont un coût économique et environnemental directement lié au contrôle de ces dernières(Schreinemachers et Tipraqsa, 2012). Le contrôle des pullulations de rongeurs via l'utilisation de rodenticides pose la question de l'impact de ces traitements sur la faune non-cible et les populations humaines lors des transferts de contaminant par consommation de proies empoisonnéesSage et al., 2008;Berny et al., 2010; Coeurdassier et al., 2012; Gabriel et al., 2012;Jacquot et al., 2013;Coeurdassier et al., 2014;Montaz et al., 2014;López-Perea et al., 2015) (Figure 6). ...
... To date, the few studies available have shown very variable patterns of exposure for NTSM. 3% ), 23% (Geduhn et al. 2014) and ~50% (Brakes and Smith 2005;Sage et al. 2008) of the specimens analyzed were exposed to ARs. A better understanding of the drivers of such variability would improve the assessment of both exposure and risk for small mammals themselves and also for their predators. ...
... Its home range, mobility, dispersal, and/or diet may be influenced by the densities of the population itself and those of interacting species (see for instance (Yunger et al. 2002;Bujalska et al. 2009), seasons, notably during breeding and non-breeding periods (Quéré and Le Louarn 2011) or gender and age (Borowski 2003;McDevitt et al. 2014). For instance, Sage et al. (2008) showed that female water voles had greater bromadiolone concentrations in tissues than males and assumed that this could be due to the lower mobility of females which would be thus more exposed to local baits. However, knowledge about whether such factors determine exposure of small mammals to ARs remains inconsistent and the potential influence of population density and interacting species has never been investigated. ...
... Notation day −1 stands because of the daily time resolution. Such quantity, C, was available for voles, and a proportion disappeared in the environment at rate k 0 (set at k 0 = 0.0815) (Sage et al., 2008). ...
... The absorption rate of ARs (η) exceeds 50% in less than 24 hr (Jacquot et al., 2013). The excretion rate from voles, k out , V was 0.4/day (Sage et al., 2008). The mortality rate through ARs was µ(D V ). ...
Article
1. Understanding pesticide impacts on populations of target/non‐target species and communities is a challenge to applied ecology. When predators that otherwise regulate pest densities ingest prey contaminated with pesticides, this can suppress predator populations by secondary poisoning. It is, however, unknown how species relationships and protocols of treatments (e.g. anticoagulant rodenticide (AR)) interact to affect pest regulation. 2. To tackle this issue, we modelled a heuristic non‐spatialized system including montane water voles, specialist vole predators (stoats, weasels), and a generalist predator (red fox) which consume voles, mustelids and other prey. By carrying out a broad‐range sensitivity analysis on poorly known toxicological parameters, we explored the impact of 5 farmer functional responses (defined by both AR quantity and threshold vole density above which AR spreading is prohibited) on predator‐prey interactions, AR transfer across the trophic chain and population effects. 3. Spreading AR to maintain low vole densities suppressed mustelid and fox populations, leading to vole population dynamics being entirely regulated by AR use. Such vole‐suppression treatment regimes inhibited predation ecosystem services and promoted pesticide dependence. 4. Keeping vole density below acceptable bounds by spreading AR while maintaining sufficient voles as prey resources led to less AR being applied and extended periods without AR in the environment, benefiting predators while avoiding episodes with high vole density. This may meet farm production interests while minimizing the impact on mustelid and fox populations and associated ecosystem processes. These alternating phases of mustelids and farmer regulation highlight the consequence of intraguild relationship where mustelids may rescue foxes from poisoning. Both global and wide‐range sensitivity analysis illustrate the tightrope between predator‐prey regulation and pesticide‐pest regulation. 5. Synthesis and applications Different pesticide protocols lead to a rich variety of predator prey dynamics in agro‐ecosystems. Our model reveals the need to maintain refuges with sufficient non‐poisoned voles for sustaining specialist mustelids, to conserve the predator community given the potential of secondary poisoning with rodenticides. We suggest that long periods without pesticide treatment are essential to maintain predator populations, and that practices of pesticides use that attempt to permanently suppress a pest over a large scale are counterproductive.
... To date, the few studies available have shown very variable patterns of exposure for NTSM. 3% ), 23% (Geduhn et al. 2014) and ~50% (Brakes and Smith 2005;Sage et al. 2008) of the specimens analyzed were exposed to ARs. A better understanding of the drivers of such variability would improve the assessment of both exposure and risk for small mammals themselves and also for their predators. ...
... Its home range, mobility, dispersal, and/or diet may be influenced by the densities of the population itself and those of interacting species (see for instance (Yunger et al. 2002;Bujalska et al. 2009), seasons, notably during breeding and non-breeding periods (Quéré and Le Louarn 2011) or gender and age (Borowski 2003;McDevitt et al. 2014). For instance, Sage et al. (2008) showed that female water voles had greater bromadiolone concentrations in tissues than males and assumed that this could be due to the lower mobility of females which would be thus more exposed to local baits. However, knowledge about whether such factors determine exposure of small mammals to ARs remains inconsistent and the potential influence of population density and interacting species has never been investigated. ...
... Bromadiolone is a highly cumulative poison and elimination tends to be very slow. It has a relative long duration of action, with sub-lethal residues still persisting up to 135 days in voles (Sage et al. 2008). ...
... Due to its persistence bromadiolone may poses a secondary poisoning risk, particular after large fieldbaiting programs (Berny et al. 1997, Giraudoux et al. 2006, Sage et al. 2008. In laboratory research owls have died after eating poisoned rats (Rattus sp.) , although only a small number of stoats (Mustela erminea) and no buzzards (Buteo sp.) died when fed poisoned voles. ...
... Anticoagulant rodenticides have been reported as a significant risk for non-target species that may consume the toxic bait (primary poisoning) or by secondary poisoning when predators eat contaminated prey (Berny et al., 1997;Shore et al., 2003;Brakes and Smith, 2005;Sage et al., 2008;Sarabia et al., 2008;Walker et al., 2008;Olea et al., 2009;Winters et al., 2010). Chlorophacinone, despite being a firstgeneration rodenticide, has been shown to have secondary toxicity among raptors, owls, mustelids, and foxes (Mendenhall and Pank, 1980;Albert et al., 2010;Fournier-Chambrillon et al., 2004). ...
... Massive poisoning with first-generation rodenticides is still relatively harmless when compared with the large scale use of the more persistent secondgeneration rodenticides, which imply a higher risk of secondary Table 1 Details about parasites and pathogens in chlorophacinone exposed and flocoumafen intoxicated bustards, and comparison with non-intoxicated individuals. poisoning for scavengers and predators (Berny et al., 1997;Walker et al., 2008;Sage et al., 2008). There was a clear correlation between the curve reflecting presence of chlorophacinone in dead bustards through the last 10 years and vole peaks at an area of Castilla y León where rodenticide use was allowed, just 70 km northwest from our main study site in northeastern Madrid (Fargallo et al., 2009). ...
Article
For many years anticoagulant rodenticides have been used in vole control campaigns, in spite of the proven risk of secondary poisoning of non-target predators and scavengers. In this paper we analyse for the first time great bustard exposure and intoxication by anticoagulant rodenticides in Spain, based on residues found in the livers of 71 bustard carcasses collected during 1991-2010. Ten individuals contained chlorophacinone and one flocoumafen. Chlorophacinone level was significantly correlated with the pathogen and parasite burden of intoxicated birds. Moreover, through the last 12 years the annual number of great bustards that present chlorophacinone in liver collected in our study areas was correlated with vole peaks at a nearby area, suggesting that the ingestion of rodenticide was proportional to the amounts spread in the fields. We conclude that rodenticide consumption is a regular event among great bustards when baited cereal is spread on fields, and that this may cause chronic weakening of intoxicated individuals, possibly affecting their survival. Future rodent control actions should consider these negative side effects on non target granivorous steppe and farmland species, particularly when they are globally threatened.
... Each individual symbol represents one mouse concentrations in those mice with detectable residues in the present study were some two-three orders of magnitude lower than the dietary concentrations of bromadiolone, difenacoum and flocoumafen that caused some mortality in owls and 5-10fold lower than the concentrations of brodifacoum that cause mortality. Whole body rodenticide concentrations in these mice would be expected to be lower as the liver tends to contain the bulk of the rodenticide that is sequestered in the body (Giraudoux et al. 2006;Sage et al. 2008) but constitutes only *5 % of body mass (this study). Given this and that only 14 % of rodents contained detectable rodenticides, it would appear that the risk of secondary poisoning to predators of wood mice some 2-3 months after the onset of baiting is low. ...
... This would result in a greater secondary exposure and poisoning risk to predators, but we have no information on how the abundance and availability of such animals to predators may have changed following onset of baiting on our study farms. Sage et al. (2008) found that the greatest numbers of contaminated water voles (Arvicola terrestris), the target species, were found within 2-3 weeks of the onset of extensive baiting. It is possible that, similarly, there is a time-window of high risk of secondary exposure and poisoning on farms during the first couple of weeks after onset of baiting, but this may be localised to farm buildings and not persist. ...
Article
We compared capture rates and exposure to SGARs of wood mice (Apodemus sylvaticus) and house mice (Mus domesticus) in autumn/winter on farms that currently used, had previously used, and never used SGARs. 6-10 weeks after baiting programmes began, 15 % of 55 wood mice and 33 % of 12 house mice had detectable liver SGAR residues. Wood mice with residues occurred on farms not using rodenticides, reflecting the high mobility of these animals, and four had multiple liver residues, possibly due to cross-contamination of baits. The winter decline in wood mouse numbers was similar on farms that did and did not use SGARs, suggesting little long-term impact of SGARs on populations on farms. Our results indicate residual levels of rodenticides will be ever present in small mammal prey across the agricultural landscape unless all farms in a locality cease application. The implications for secondary exposure and poisoning of predators are discussed.
... While some species that depend on agro-ecosystems are declining (Aviron et al., 2009), others are outbreaking according to specific time laps and are considered as agricultural pests Koyanagi et al., 2012;Krebs, 2013). Small mammal pests, including some grassland voles (e.g. the montane water vole (Arvicola scherman) and the common vole (Microtus arvalis)), have been widely studied with concern about agricultural economy, ecotoxicology, eco-epidemiology and fundamental ecology (Parshad, 1999;Hanski et al., 2001;Zhang et al., 2003;Korpimäki et al., 2004;Giraudoux et al., 2006;Sage et al., 2008;Sluydts et al., 2009;Wang et al., 2010;Decors et al., 2011;Fraschina et al., 2012;Gabriel et al., 2012). ...
... Localisation d'exemples de pullulations de micro-mammifères dans le monde.Ces « pestes agricoles » ont un coût économique et environnemental directement lié au contrôle de ces dernières(Schreinemachers et Tipraqsa, 2012). Le contrôle des pullulations de rongeurs via l'utilisation de rodenticides pose la question de l'impact de ces traitements sur la faune non-cible et les populations humaines lors des transferts de contaminant par consommation de proies empoisonnéesSage et al., 2008;Berny et al., 2010; Coeurdassier et al., 2012; Gabriel et al., 2012;Jacquot et al., 2013;Coeurdassier et al., 2014;Montaz et al., 2014;López-Perea et al., 2015) (Figure 6). ...
... Wheat baits were industrially prepared at a constant concentration of 50 mg kg À1 during the study period. Baits were distributed in artificial linear burrows (details in Sage et al. 2008). Legislation limits the quantity of baits used per treated area to a maximum of 20 kg ha À1 . ...
... The first measure would be to reduce the maximum bait quantity authorized per ha. Sage et al. (2008) and Coeurdassier et al. (2012) demonstrated that treatments performed at bait densities of 20 kg ha À1 (i.e. the highest quantity authorized by regulation) presented a high risk to predators of voles. In the present study, we showed that fox populations were affected even if less than 8Á4 kg ha À1 of bait was used across 96% of the treated area. ...
Article
Pest control is a global issue for agriculture, health, biodiversity conservation and economy. Anticoagulant rodenticides are used over large areas to control rodent pests and can cause widespread poisoning of nontarget wildlife. In France, bromadiolone is the only pesticide authorized to control the water vole Arvicola terrestris Scherman, in grasslands. Since 2001, legislation has been in place to replace curative treatments by preventive ones and limit the quantity of rodenticide used. As the legislation took effect over time, the impact on red fox Vulpes vulpes populations was monitored.Fox populations and bromadiolone treatments were monitored in the Doubs Department (5000 km² area), France. Fox counts were carried out during spring, and vole control was primarily conducted in autumn. Relative fox densities (Kilometric Abundance Index: KAI) obtained per commune for year n (2004–2009) were related to treatments achieved during year n−1 (2003–2008). Treatments from year n−2 were used to investigate possible delayed responses in fox populations.Kilometric Abundance Index of foxes was significantly related to treatment intensities in years n−1 and n−2. The impact was greatest in a large area (>1000 km²), where intensive treatments were achieved in 2003. Fox KAI generally remained dramatically low in this area until 2005, after which a partial recovery was observed.The same area was treated again from 2006 to 2008 but with only half the amount of bait per hectare that was used in 2003. These treatments were followed by a moderate decrease in fox populations.Synthesis and applications: We have established, for the first time on a regional scale, the negative impact of a rodenticide on fox populations. We have shown that a shift to preventive treatments with reduced anticoagulant rodenticide use is less harmful to fox populations. However, to approach a zero impact, treatments should be reduced further by limitation of bait quantities authorized per hectare and per commune and using alternative methods to chemical control. Long-term monitoring of wildlife populations using index methods can provide valuable information about the adverse effects of pesticides; therefore, we recommend their inclusion in the assessment of pest management practices.
... To date, the few studies available have shown very variable patterns of exposure for NTSM. 3% ), 23% (Geduhn et al. 2014) and ~50% (Brakes and Smith 2005;Sage et al. 2008) of the specimens analyzed were exposed to ARs. A better understanding of the drivers of such variability would improve the assessment of both exposure and risk for small mammals themselves and also for their predators. ...
... Its home range, mobility, dispersal, and/or diet may be influenced by the densities of the population itself and those of interacting species (see for instance (Yunger et al. 2002;Bujalska et al. 2009), seasons, notably during breeding and non-breeding periods (Quéré and Le Louarn 2011) or gender and age (Borowski 2003;McDevitt et al. 2014). For instance, Sage et al. (2008) showed that female water voles had greater bromadiolone concentrations in tissues than males and assumed that this could be due to the lower mobility of females which would be thus more exposed to local baits. However, knowledge about whether such factors determine exposure of small mammals to ARs remains inconsistent and the potential influence of population density and interacting species has never been investigated. ...
Chapter
Full-text available
Both target and non-target small mammals are exposed to rodenticides (AR). A better understanding of the drivers controlling this exposure is critical for the conservation of threatened small mammal species but also because they may represent important pathways of poisoning for birds of prey and carnivore mammals. Here, we consider the spatial components involved in the process of small mammal exposure to ARs with the aim to address how these can be used in spatially explicit risk assessment. We present how various drivers operate on multiple spatial scales. On continental and/or regional scales, both biogeographical distribution of small mammals and other species of conservation value and international/national regulations of AR applications (indoor vs outdoor…) could be used to identify some countries or states where exposure is more likely. For application at the local scale (i.e. few km²), we reviewed published studies that analysed the spatial pattern of small mammal exposure to ARs according to species and distance to treatments. We evidence that most of the small mammals exposed to AR are found in the immediate vicinity of treatment areas, i.e., within 100 m. Over 100 m, exposed rodents are rare but can be found until 750 m distance from treatment areas. Species traits related to spatial dimension such as habitat preferences, home range size and mobility also influence exposure. Exposure is variable, in terms of proportion of contaminated individuals and levels of residues, for species showing small home-range size and a limited spatial mobility. The level of exposure depends on whether the main habitat of the given species is similar or not to the one of the target rodent. For instance, exposure of the common vole, a grassland species, is low when ARs are used indoor while it can be highly exposed when bromadiolone is applied outdoor to control the water vole, a sympatric species. For small mammals exhibiting a relatively large home-range size and a high spatial mobility such as the wood mouse and the bank vole, the exposure is commonly reported within a lower range than target species. Although this has not been studied in details, we also address how landscape and/or habitat features may modulate exposure, suggesting that landscape management may help to mitigate the risk of ARs to small mammals. Finally, we discuss both the advantages and disadvantages of statistical, analytical or simulation models to assess potential or actual exposure of NTSM to AR in a spatially explicit way. We conclude that in order to analyse global patterns in usage and exposure risks, large scale statistical modelling should be used while for detailed site specific assessments, simulation models may be more appropriate.
... Although we detected no seasonal differences in exposure in liver samples, the long hepatic half-lives of second-generation ARs likely obscured our ability to detect seasonal differences. Additionally, because second-generation ARs may persist in small mammal species from 90 to 135 days after removal of poison baits, poisoned small mammals may remain a continuing source of exposure for predatory species long after the end of poisoning programs (Murphy et al. 1998;Sage et al. 2008). ...
Article
Full-text available
Anticoagulant rodenticides (ARs) are increasingly recognized as a threat to nontarget wildlife. High exposure to ARs has been documented globally in nontarget predatory species and linked to the high prevalence of an ectoparasitic disease, notoedric mange. In southern California, mange associated with AR exposure has been the proximate cause of a bobcat (Lynx rufus) population decline. We measured AR exposure in bobcats from two areas in southern California, examining seasonal, demographic and spatial risk factors across landscapes including natural and urbanized areas. The long-term study included bobcats sampled over a 16-year period (1997-2012) and a wide geographic area. We sampled blood (N = 206) and liver (N = 172) to examine exposure ante- and post-mortem. We detected high exposure prevalence (89 %, liver; 39 %, blood) and for individuals with paired liver and blood data (N = 64), 92 % were exposed. Moreover, the animals with the most complete sampling were exposed most frequently to three or more compounds. Toxicant exposure was associated with commercial, residential, and agricultural development. Bobcats of both sexes and age classes were found to be at high risk of exposure, and we documented fetal transfer of multiple ARs. We found a strong association between certain levels of exposure (ppm), and between multiple AR exposure events, and notoedric mange. AR exposure was prevalent throughout both regions sampled and throughout the 16-year time period in the long-term study. ARs pose a substantial threat to bobcats, and likely other mammalian and avian predators, living at the urban-wildland interface.
... La lutte contre le campagnol terrestre a été rendue obligatoire dans le département du Doubs depuis le 28 décembre 2015 et dans le département du Jura depuis le 29 décembre 2015. Afin de limiter l'usage de rodenticides pouvant impacter la faune non cible (Brakes & Smith 2005 ;Giraudoux et al. 2006 ;Sage et al. 2008), des éléments de lutte raisonnée ont été mis en place (Couval & Truchetet 2014). L'abondance des campagnols étant connue pour diminuer lorsque la pression de pâturage augmente, l'alternance entre des régimes de fauche et de pâturage est préconisée (Jacob 2003 ;Morilhat et al. 2007). ...
Thesis
En Europe, les prairies semi-naturelles de moyenne montagne sont principalement des écosystèmes ayant évolués au cours de plusieurs décennies d’activité humaine. Ces écosystèmes présentent une biodiversité remarquable et dépendent de régimes traditionnels de perturbations par la fauche ou le pâturage. Cependant, dans l’objectif d’augmenter leur production de fourrage, les prairies semi-naturelles sont soumises à des régimes de perturbations de plus en plus importants ainsi qu’à de nouveaux types de perturbations. Ce travail de thèse propose d’apporter de nouveaux éléments pour suivre et comprendre l’impact des perturbations sur la diversité des communautés végétales des prairies semi-naturelles.Dans un premier temps, la comparaison de relevés de végétation anciens (2005 à 2009) avec des relevés récents (2019) a été réalisée dans des prairies de fauche de moyenne montagne. Cette comparaison a permis de mettre en évidence des évolutions contrastées de la diversité végétale et des régimes de perturbations entre deux massifs. Dans le massif des Vosges, la diversité végétale ainsi que les régimes de perturbations ne semblent pas avoir évolué. A l’inverse, dans le massif du Jura, la diversité végétale a fortement diminué, probablement en association avec une augmentation de la fréquence des régimes de perturbations et de la fertilisation.Dans un second temps, l’impact de perturbations de forte intensité sur la diversité végétale a été évalué. Dans les prairies de fauche, les perturbations par les pullulations de campagnols terrestres semblent permettre une augmentation de la richesse spécifique par la réduction de la compétition pour la lumière. A l’inverse, ces perturbations semblent favoriser des espèces proches phylogénétiquement et entraîner une diminution de l’équitabilité phylogénétique. Dans les pelouses sèches, les perturbations par l’utilisation de broyeurs de pierres ne semblent pas impacter la diversité végétale. En revanche, la composition en espèces des milieux perturbés évolue vers des végétations de prairies productives suite à la perte des espèces typiques des pelouses.Dans un troisième temps, l’utilisation d’espèces diagnostiques comme indicateurs des régimes de perturbations et de la diversité végétale dans les prairies pâturées du massif du Jura a été testée. Le nombre d’espèces diagnostiques dans un relevé de végétation s’est révélé être un bon indicateur de la diversité végétale et des régimes de fertilisation. Cependant, les espèces diagnostiques ne semblent pas être de meilleurs indicateurs que des espèces généralistes des prairies pour évaluer l’intensité des régimes de perturbations.Nos résultats confirment que les changements de pratiques agricoles sont une menace majeure pour la diversité végétale des prairies semi-naturelles de moyenne montagne, en particulier dans le massif du Jura. Nos travaux mettent également en avant que l’augmentation de la fréquence des régimes de perturbations est susceptible d’avoir davantage d’effets négatifs sur la diversité végétale que des perturbations de forte intensité mais peu fréquentes. Néanmoins, certaines perturbations de forte intensité, comme l’utilisation de broyeurs de pierres, peuvent entraîner des modifications très importantes et irréversibles de la composition en espèces des milieux perturbés. Dans l’objectif de concilier enjeux sociétaux et environnementaux, il convient de maintenir des parcelles productives ou les régimes de perturbations par la fauche ou le pâturage sont fréquents, ce qui permet d’assurer une production fourragère importante. Cependant, Il est également nécessaire de limiter la fréquence et l’intensité des perturbations dans des parcelles encore peu intensifiées afin de protéger leur composition en espèces ainsi que leur diversité végétale.
... a b s t r a c t a r t i c l e i n f o rodenticides (ARs), which makes these predators susceptible to secondary poisoning by AR-contaminated prey (Brakes and Smith, 2005;Sage et al., 2008;Rattner et al., 2014b). In the last decades, several studies have been performed that reveal the prevalence of exposure in nontarget wildlife species at risk. ...
Article
We studied the prevalence of anticoagulant rodenticides (ARs) in the liver of 344 individuals representing 11 species of predatory wildlife that were found dead in the Mediterranean region of Spain (Catalonia and Majorca Island). Six different ARs (brodifacoum, bromadiolone, difenacoum, flocoumafen, difethialone, warfarin) were found in the liver of 216 (62.8%) animals and >1 AR co-occurred in 119 individuals (34.6%). The occurrence of ARs was positively correlated with the human population density. Catalonia and Majorca showed similar prevalence of AR detection (64.4 and 60.4%, respectively), but a higher prevalence was found in the resident population of Eurasian scops owl (Otus scops) from Majorca (57.7%) compared to the migratory population from Catalonia (14.3%). Birds of prey had lower levels of bromadiolone than hedgehogs, whereas no difference was found for other ARs. The risk of SGAR poisoning in wild predators in NE Spain is believed to be elevated, because 23.3% of the individuals exhibited hepatic concentration of ARs exceeding 200ng/g. Copyright © 2014 Elsevier B.V. All rights reserved.
... Indeed, international authorities have stressed the need for environmental risk assessment regarding the use of these pesticides in the field, especially with regard to their transfer in food chains. Moreover, anticoagulant residues in wildlife have been shown to be increased by survey programs over the last years, leading to greater concerns of non-target effects (Sage et al. 2008). ...
Article
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The use of anticoagulants has increased in recent times as a method for controlling rodent populations. However, this increased use also provokes accidental and intentional ingestion for both animals and humans, triggering poisoning of non-target organisms. In the present report, a clinical case of secondary-poisoning of birds with anticoagulant rodenticides, which took place after a general rodenticide treatment in an Ornithological Zoological Park, is described. Three birds died as a result and samples were submitted to the Veterinary Hospital in Lugo (Galicia, NW Spain). After necropsy, samples of the birds, together with molluscs and faeces, were submitted to the Toxicology Unit of Caceres (Extremadura, W Spain) in order to detect possible chemicals. Results from HPLC analyses revealed the presence of the rodenticides difenacoum and brodifacoum. The present report shows that the risk of secondary exposure resulting from the scavenging of molluscs is likely to be significant. The potential routes of uptake by invertebrates include the consumption of rodent faeces, rodent carcases, the ingestion of soil-bound residues, and the direct consumption of poison baits.
... Therefore, the environmental stability plus the elevated persistence of bromadiolone in rodents after field controls carry a significant risk of poisoning on predatory species (Giraudoux et al., 2006). After field control operations with bromadiolone against water voles in France, 99.6% of water voles (Arvicola amphibius) trapped underground and 41% of common voles (Microtus arvalis) trapped above ground contained AR residues in liver, in some cases 135 days after treatment (Sage et al., 2008). ...
... Also, it is effective against warfarin-resistant rats and mice, including Norway rats (R. norvegicus) (1)(2)(3). B residues have been detected in tissues of Arvicola terrestris (4)(5)(6) and coypu (Myocastor coypus) (7) after field use. Its main activity is the vitamin K epoxide reductase inhibition, an enzyme that causes blood clotting alteration and hemorrhages leading to death. ...
Article
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Cereal-based bromadiolone anticoagulant is often used for rodent control, and because these baits are attractive for poultry they may be accidentally ingested. Thus, the aim of this study was to develop a new high-performance liquid chromatography (HPLC) method for the determination of bromadiolone residues in hens' eggs and its plasma kinetics. Laying hens (n = 48) were divided into four groups of 12 animals each. Groups I and II received orally a single dose of bromadiolone 10 mg/kg, group III received a single dose of bromadiolone 60 mg/kg, and group IV was the control. Eggs were collected from groups I, III, and IV, whereas plasma was collected from groups II and IV. The HPLC method developed was reproducible, sensitive, accurate, and linear within the range 0.1-20 µg/g. The final HPLC conditions were as follows: mobile phase MeOH-ammonium acetate (0.5 M) triethylamine buffer (pH 5, 51:49, v/v); analytical column Luna C18 ODS2; wavelength 260 nm; flow rate of 1.5 mL/min; and warfarin as internal standard (5 µg/mL). Recoveries for bromadiolone were in the range of 72–80% with RSD lower than 10%. Pharmacokinetic behavior of bromadiolone in hens results faster than that reported in other animals and humans. Following 10 and 60 mg/kg treatment bromadiolone was not detected in albumen but was present in yolk from day 4 to 5 and from day 2 to 9. In conclusion, the bromadiolone amount found in eggs was well below the toxic dose of this anticoagulant for humans, and no anticoagulant effect should be observed.
... So, on each exposure day, captive foxes were fed 5 water voles trapped in an area that had never been treated with bromadiolone before (no bromadiolone residues were detected in liver of 5 randomly sampled voles). Foxes that were to be dosed with bromadiolone were fed voles that had been spiked with a quantity of bromadiolone similar to that found in voles during 20 days after treatment in a field study (Sage et al., 2008). ...
Article
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In many countries, the fox (Vulpes vulpes), predator of small mammals, is particularly affected by anticoagulant rodenticides such as bromadiolone due to secondary poisoning. Nevertheless, to date, no method of exposure monitoring is applicable in the field over large areas, and no toxicological data are available concerning sensitivity of foxes to bromadiolone. The aim of this work was to compare excretion kinetics of bromadiolone in fox faeces with clinical and haemostatic effects after repeated exposure to intoxicated voles. A sensitive method for the quantification of bromadiolone excretion in fox faeces and plasma was developed, using liquid chromatography combined with electrospray ionisation mass spectrometry (LC/ESI-MS). The LoD was 0.9microg/kg and 0.15microg/L, and the LoQ was 3.0microg/kg and 0.5microg/L, in faeces and in plasma, respectively. Four captive foxes were fed for 2 or 5 days with water voles (Arvicola terrestris Sherman) spiked with bromadiolone at concentrations close to those measured in the field. Faeces and blood were collected for bromadiolone titration, and blood-clotting tests were performed to monitor fox health daily during 10 days and then every 3-4 days until the end of the experiment (D28). Then, after euthanasia, a complete necropsy was performed, and levels of bromadiolone residues in the liver were determined. Bromadiolone residues were detected in faeces 15h after the first exposure. They increased dramatically during the exposure period and then gradually decreased, but they remained detectable at the end of the experiment, i.e., 26 days after the last exposure. Bromadiolone residues in plasma showed a similar pattern but were no longer detectable 7-24 days after the last exposure. Two foxes presented very severe external haemorrhages, requiring the administration of the antidote vitamin-K1. Bromadiolone residues in faeces and their relationships with exposure and other direct-markers that were measured are discussed. Liver residues and the toxicity data of our study will help to interpret data from fox carcasses collected by wildlife disease surveillance networks. These findings provide a basis for programs aiming to monitor the exposure of wild fox populations to bromadiolone using non-invasive methods based on standard sampling and analysis of residues in faeces.
... Second-generation ARs (SGARs) generally present more physiological persistence in vertebrate livers than their first-generation counterparts (Thomas et al., 2011). In any case, rodents exposed to SGARs survive for several days and will continue feeding on baits (Sage et al., 2008). The consumption of poisoned rodents by predatory animals can cause secondary poisoning in predators and result in the mortality of non-target species. ...
... However, other tissues of the carcasses also contain residues. Sage et al., 2008 found about 25% of whole body bromadiolone residues in the liver of water voles. Assuming similar residue distribution of BR in the small mammals considered in this study, the absolute risk for barn owls would be 4 times higher than stated. ...
Article
Worldwide, small rodents are main prey items for many mammalian and avian predators. Some rodent species have pest potential and are managed with anticoagulant rodenticides (ARs). ARs are consumed by target and non-target small mammals and can lead to secondary exposure of predators. The development of appropriate risk mitigation strategies is important and requires detailed knowledge of AR residue pathways. From July 2011 to October 2013 we collected 2397 regurgitated barn owl (Tyto alba) pellets to analyze diet composition of owls on livestock farms in western Germany. 256 of them were fresh pellets that were collected during brodifacoum baiting. Fresh pellets and 742 liver samples of small mammals that were trapped during baiting in the same area were analyzed for residues of ARs. We calculated exposure risk of barn owls to ARs by comparing seasonal diet composition of owls with AR residue patterns in prey species. Risk was highest in autumn, when barn owls increasingly preyed on Apodemus that regularly showed AR residues, sometimes at high concentrations. The major prey species (Microtus spp.) that was consumed most frequently in summer had less potential to contribute to secondary poisoning of owls. There was no effect of AR application on prey composition. We rarely detected ARs in pellets (2 of 256 samples) but 13% of 38 prey individuals in barn owl nests were AR positive and substantiated the expected pathway. AR residues were present in 55% of 11 barn owl carcasses. Fluctuation in non-target small mammal abundance and differences in AR residue exposure patterns in prey species drives exposure risk for barn owls and probably other predators of small mammals. Exposure risk could be minimized through spatial and temporal adaption of AR applications (avoiding long baiting and non-target hot spots at farms) and through selective bait access for target animals.
... Ce déficit d'études et de données est encore plus important pour les contaminants organiques. Ainsi, à part les travaux de notre unité portant sur le devenir in situ de la bromadiolone et de son transfert chez le campagnol terrestre, le campagnol des champs et le renard roux (Giraudoux et al., 2006 ;Sage et al., 2007Sage et al., , 2008, les données sur des polluants tels que les HAPs, les PCBs, les LAS (linear alkylbenzene sulfonate) sont très rares sur des sites français ou européens. Nous présentons des résultats obtenus sur le campagnol roussâtre, une des espèces de micromammifères échantillonnées autour de l'ancien site métallurgique Metaleurop du Nord de la France étudié dans le cadre du programme STARTT. ...
... Up to 73% of dead poisoned muskrats (Ondatra zibethicus) were detected above ground, increasing the risk of secondary poisoning (Tuyttens & Stuyck 2002). According to Sage et al. (2008) storing of baits by water voles increases the persistence of bromadiolone even up to 10 times. This could also lead to a delayed exposure of rodent predators during a possible recolonization by voles. ...
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Anticoagulant rodenticides are the principal means of controlling pest rodents in the Nordic countries. Due to the intrinsic properties of second generation anticoagulants, i.e. extremely slow elimination from the body and high toxicity, they are prone to accumulate in the non-target species which consume poisoned rodents. Despite wide use there are no published studies on occurrence of residues of anticoagulant rodenticides in the non-target animals in the Nordic countries. This review of publicly available studies was aimed to find out which anticoagulant substances are found and in which species. The concentrations are reported as well as the proportion of exposed animals. We have further compiled a list of species that could potentially be exposed to anticoagulant rodenticides in the Nordic countries. The review shows that anticoagulant residues have been found everywhere they have been measured and secondary exposure to second generation anticoagulants is common among certain avian and mammalian predators. The results call for initiation of measurements of anticoagulant rodenticides also in the Nordic countries.
... Despite a mountainous terrain, a wildlife conservation policy, and low human activities, a number of wildlife species was exposed to ARs in the PNP, with risk of exposure matching more-inhabited areas. As previously described (Grolleau et al. 1989;Lefebvre et al. 2017), our results show that species that regularly consume small mammals were more exposed to ARs, supporting exposure of nontarget wildlife secondary to the ingestion of poisoned rodents (Sage et al. 2008;López-Perea and Mateo 2018). Among those species, the highest risk of AR exposure was found in red fox (62%, 21/34). ...
Article
The extensive use of anticoagulant rodenticides (ARs) to control rodent populations poses intoxication risks for wildlife: persistence of ARs in rodents can cause secondary exposure and poisoning of predators or scavengers. We investigated risk factors for wildlife exposure to ARs in the Parc National des Pyrénées (PNP), France, using a multivariable logistic regression analysis. A total of 157 liver samples were collected from carcasses of 10 mammal and three bird species found in the PNP between 2010 and 2018 and screened for presence of AR residues. First- and second-generation ARs were detected in more than 60% of red fox (Vulpes vulpes) and stone marten (Martes foina) samples and in around 40% of wild cat (Felis silvestris), European pine marten (Martes martes), American mink (Neovison vison), and Eurasian Buzzard (Buteo buteo) samples. Wildlife exposure to ARs was significantly associated with consumption of small mammals (odds ratio [OR]: 2.5, 95% confidence interval [CI]: 1.1-5.8) being collected in the Ossau valley (OR: 2.5, 95% CI: 1.1-6.1) and between 2013 and 2015 (OR: 4.8, 95% CI: 2.0-11.7). We identified wild species that could be targeted for risk-based surveillance program for AR secondary exposure and determined high risk areas in which alternative measures should be applied for rodent control.
... Some species that are secondarily exposed through predation on rodents, or exposed at the tertiary level or further, such as mesopredators like coyotes (Canis latrans) or apex predators like mountain lions (Puma concolor), do not prey on the target rodent species, leaving their route of exposure unknown. The delayed toxicity of anticoagulant rodenticides and their persistence within tissues can result in contaminated rodents being found within and adjacent to the treated area weeks or months after bait application (Sage et al. 2008, Tosh et al. 2012, Geduhn et al. 2014. ...
Article
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Anticoagulant rodenticides have been detected in many species of wildlife worldwide. However, the origins, exposure pathways, and effects of this exposure are not well understood. To accurately characterize the risks to wildlife from rodenticide use, better information is needed regarding the proportion of populations being exposed, what proportion of individuals in populations are affected, and in what ways. The relationship between anticoagulant rodenticide concentrations found in wildlife and the rate of mortality or illness have been the subjects of much research. Residue levels observed in liver and whole-body analyses vary and overlap extensively among apparently healthy asymptomatic individuals and sublethal and lethal cases. Results from laboratory studies also show there can be wide variability in lethal and sublethal effects among and within taxonomic groups. Correlating the sublethal and reproductive effects observed in laboratory studies with realistic exposure scenarios and effects in the wild is needed to improve risk assessments. For species with limited numbers or declining populations, a critical question yet to be answered is if the rodenticide exposure documented in individual animals inhibits population growth or contributes to population declines by lowering survival and reproductive success. This information is essential to the regulatory agencies that must weigh the risks and benefits of rodenticide uses and identify restrictions that are effective in reducing risks to wildlife.
... Some intensive island rat control operations in New Zealand caused large (>90%) reductions or total extirpation of indigenous rails, such as Weka, and declines in other species that also fed directly on baits (see Eason and Spurr (1995) for review, also Pitt et al. (2015)). Primary exposure of mainland nontarget small mammal populations around baited agricultural premises and baited grasslands can also lead to reductions in numbers (Brakes and Smith, 2005;Cox and Smith, 1990;Geduhn et al., 2014;Sage et al., 2008). Impacts on island nontarget populations, where opportunities for recruitment through immigration may be limited, will depend on the number of animals that survive rat control operations and their subsequent rate of reproduction. ...
Chapter
Rodents are controlled because of the human health and economic threats they pose. Anticoagulant rodenticides (ARs) are the most widely used control agent and work by interrupting the vitamin K cycle, ultimately impairing blood clotting. Various “first-generation anticoagulant rodenticides” (FGARs) were developed in the 1950s and 1960s but, following the development of resistance in rats and mice, have been superseded in many countries by second-generation anticoagulant rodenticides (SGARs), to which there is currently only limited resistance. Collectively, SGARs are the most widely used chemicals for rodent control throughout the world, although FGAR use still remains. AR use is regulated in many countries, not least because it poses an environmental risk. This is because ARs are toxic to all vertebrates, including nontargets—species not subject to control campaigns. Exposure occurs typically as a result of ingestion, consumption either of bait (primary exposure) or of live or dead (target or nontarget) prey species that have fed on baits (secondary exposure). Animals most at risk of primary exposure include invertebrates, reptiles, birds and mammals, and granivorous (grain-feeding) species are the most likely to be attracted to and feed on grain-based baits. Most environmental studies have focused on secondary exposure to SGARs; the greater acute toxicity and persistence in (prey) body tissues of these compounds, compared with FGARs, enhances the likelihood of secondary exposure and poisoning. Such exposure is often detected from the presence of liver residues and indicates occurrence of one or more exposure events. Many studies on secondary exposure have been conducted and collectively show that exposure is widespread among predatory and scavenging species throughout the world. In some species, almost all individuals in a population may have liver residues, and detection of multiple compounds is common. This suggests predators and scavengers commonly experience repeated, sublethal, exposures, and ARs are transferred through multiple food webs. The amount of use, baiting practices, dietary preferences, the presence of resistance, and competition for food resources, are some of the factors that influence the likelihood of exposure. A critical question is what are the effects of exposure in nontarget individuals and populations? Most information is available about acute mortalities in vertebrates, although definitive attribution of cause of death to ARs, based on necropsy sign and the presence of chemical residue, is challenging. Despite such diagnostic uncertainties, there is evidence that use of ARs does result in some wildlife mortalities, although the extent of these varies between species, location, and baiting practices. It is documented that primary poisoning has caused reductions in population numbers in some cases. Although secondary AR poisonings can sometimes involve large numbers of individuals, there is no clear evidence to date of direct AR-mediated population declines in predators although mortalities may be a significant additional population stressor. While most concern has focused on lethal poisoning, the widespread secondary exposure that occurs in predators may possibly be associated with sublethal effects, although the extent and importance of any such effects are poorly understood and represent a major knowledge gap. Overall, the wide-scale exposure of wildlife to ARs, particularly the diverse and wide-scale secondary exposure of predators and scavengers, has led to initiatives aimed to restrict sales or implement other mitigation measures around AR use. These are intended to reduce exposure and risk among nontarget species, although their success has yet to be determined.
... two ways: (i) red kites consumed the cis-bromadiolone diastereoisomer when feeding on voles and eliminated it before dying, and/or (ii) voles had already eliminated all or most part of cis-bromadiolone diastereoisomer when they were eaten by red kites. The pharmacokinetics of bromadiolone in voles has already been documented but isomers patterns were not described (Sage et al., 2008). At present, there are no data available on the comparative pharmacokinetics of bromadiolone diastereoisomers in voles. ...
Article
Anticoagulant rodenticides (ARs) are widely used pesticides to control rodent populations. Bromadiolone, a second generation anticoagulant rodenticide (SGARs), is authorized in France to control the population of water voles (Arvicola scherman). The persistence of SGARs in rodents is responsible for secondary exposure or poisoning of predators and scavengers, and is of ecological concern for the conservation of endangered species. Commercial formulations are a mixture of two diastereoisomers of bromadiolone: 70–90% is trans-bromadiolone and 10–30% is cis-bromadiolone. Both diastereoisomers have been shown to inhibit coagulation function with the same potency. On the other hand, cis-bromadiolone has been shown to be less tissue-persistent than trans-bromadiolone in rats. This difference led to residue levels in rats with substantially weakened proportion in cis-bromadiolone compared to the composition of baits.
... Six adult foxes (mixed sex group) and that had never been exposed to ARs were individually caged, 5 were fed with Water voles spiked with ARs and 1 control was fed with uncontaminated voles. Both duration and dose of exposure of foxes to ARs were determined according to Sage et al. (2008) who showed that voles trapped in a plot treated with bromadiolone may contain over 300 g of bromadiolone per individual a few days after bait application. According to Artois (1989), adult red foxes eat 0.3-0.6 kg of food per day, which represents 4-8 water voles. ...
Article
Exposure of wildlife to anticoagulant rodenticides is mainly assessed by analysing residues in the tissues, notably liver, of dead animals. Recent finding suggested that the analysis of active ingredients in mammal scats sampled in the field could be used as a non-invasive method to monitor non-lethal exposure in populations. Here, we measure experimentally the persistence of 6 anticoagulant rodenticides in fox scats when placed under natural conditions. Six foxes were fed with voles dosed with brodifacoum, bromadiolone, chlorophacinone, warfarin, difenacoum and difethialone in controlled conditions and their faeces were collected. Then, the scats were placed outside, thus exposed to weathering, and sampled up to four months later to measure the concentrations of the 6 rodenticides. We showed that both the concentrations and the occurrence of residues in the scats decreased rapidly for all these pesticides. Based on concentrations, the degradation half-lives ranged from 5.26 days for chlorophacinone to 7.98 days for bromadiolone. Furthermore, the probability of sampling a scat containing detectable residues decreased by 10% after 7d, 2d, 10d, 5d, 3d and 10d for warfarin, chlorophacinone, bromadiolone, brodifacoum, difenacoum and difethialone respectively. Thus, in terms of using residues in scats to monitor fox exposure to rodenticides, we recommend first, to clear the studied areas of old faeces and then, sample scats after a short period, ideally <5 days.
... When voles are considered a non-target, studies have shown that in comparison to other non-targets such as field mice (Apodemus sp.) and shrews (Sorex sp.), voles are less likely to carry AR residues, however, reported residue levels in exposed individuals have been similar, and in some cases higher than other non-targets (Brakes & Smith, 2005;Elliott et al., 2014;Geduhn et al., 2014). Conversely, when voles are the target species, as is the case in central Europe where bromadiolone is applied in grasslands to combat voles, a high proportion carry bromadiolone residues after AR treatment, and residues have been found to persist in populations beyond 135 days post treatment (Sage et al., 2008). While barn owls avoided blueberry fields within their home-ranges, they would often hunt along the field margins or perch on signs and posts along the roadside verges bordering blueberry fields. ...
Chapter
In recent years anticoagulant rodenticides have emerged as an important factor reducing the survival of many birds of prey and some predatory mammals. Understanding the ecological factors driving the exposure of predators is a key component in assessing the risk posed by anticoagulant rodenticides. We have reviewed the literature to better understand and synthesize the ecological factors driving AR exposure in predators, focusing on landscape and environmental management, traits of the exposed predators and the most common exposure pathways. On a global scale, the large input of ARs into urban and agricultural settings, and the relatively large footprint of these landscapes, has led to widespread AR exposure of many species, ranging from insects to large carnivores. General inferences can be made with regards to the traits of the most affected species. We determined that at-risk predators tend to be nocturnal opportunistic species for which rodents are a key dietary component, seasonally or year-round. They also tend to be non-migratory and occupy habitats within, or in close proximity to landscapes that are heavily influenced by human activities such as intensive agriculture or urban areas. Predators that consume rats in urban environments are disproportionately affected by ARs. As our understanding of how ARs are transferred up the food-chain is still limited, there is a need to further comprehend the extent to which non-target prey are being exposed to ARs in different landscapes, as we are frequently documenting AR residues in predators that do not typically prey on rodents. We recommend a focus on urban landscapes, where to date no exposure data has been collected on non-target prey. We also have a very limited understanding of non-target prey exposure in the urban-wildland/agricultural interface where opportunistic predators are known to hunt both habitat types interchangeably. Finally, we need to decipher whether the mounting evidence of exposure in predators translates into any population level effects.
Chapter
Anticoagulant rodenticides (ARs) are currently the most common pesticides and biocides used to control rodents. The long-term persistence in animal tissues of the second-generation compounds (SGARs) causes their bioaccumulation in predatory species. In this chapter, we evaluate some of the key parameters that are likely to determine bioaccumulation and risk in wildlife from secondary exposure to ARs, review wildlife field monitoring studies from around the world to assess the scale of that exposure, and examine the current state of knowledge as to how secondary exposure relates to risk of mortality and other adverse effects in wildlife and in humans. Using a simple modelling approach and information from the published literature, we conclude that excretion rate is key in determining the extent of bioaccumulation and resultant risk in wildlife from secondary exposure to SGARs. We also find that secondary exposure in predators is widespread and widescale throughout the world, and may be greatest in predatory mammals that specialise on feeding on rodents. The extent of secondary [lethal and sub-lethal] poisoning that results is unclear. This is largely because unequivocal diagnosis of AR-mediated mortalities is not easy to determine from necropsy and there is no clear threshold residue that is diagnostic of effect, although recent development of probabilistic modelling of residue data may help in the future. We recommend that the direct consequences for predators from AR exposure, and the potential consequent impacts on the top-down regulation of rodent populations, deserve greater study.
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La structure et l’intensité des interactions ressources-consommateurs qui forment les réseaux trophiques régulent une très grande partie des transferts de biomasse mais aussi de contaminants biologiques et chimiques dans les écosystèmes. L’objectif de la thèse est de développer des modèles permettant d’étudier les mécanismes de transport des contaminants et d’évaluer ainsi d’une part la dynamique des maladies infectieuses et des pollutions chimiques, et d’autre part les réponses des réseaux trophiques soumis à ces contaminations.[...] À l’issue de ces travaux, une quatrième étape de la thèse a été d’intégrer les interactions trophiques, les dynamiques des parasites et les impacts des pollutions dans des méta-écosystèmes (i.e. avec dispersions d’individus entre écosystèmes). En utilisant la théorie des matrices aléatoires nous avons établi des mesures des risques d’émergence de parasites que nous avons évalués en fonction des perturbations extérieures.L’étude a ainsi montré que ces perturbations augmentent les risques épidémiques, mais que ces risques pouvaient être réduits par la dispersion des individus (sains et infectés) sous certaines conditions qui sont,par exemple pour les TTP, un nombre d’espèces plus grand que le nombre d’écosystèmes connectés, et un taux de virulence plus faible que le taux de contagion.Ainsi, dans un contexte planétaire d’augmentation des pressions anthropiques sur les écosystèmes,cette thèse de modélisation apporte un ensemble d’outils et de développements conceptuels permettant d’analyser quantitativement et qualitativement les transferts et les impacts des contaminants sur les écosystèmes.
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Anthropogenic activities modulate landscape and promote the establishment of invasive populations. Management of these populations represents a major issue for public health (zoonotic disease, famine), environment (biodiversity loss) and economy (damages). This multidisciplinary thesis has been conducted in natural conditions on populations of rodents infesting agricultural landscapes at large scale. This work aims to understand biological mechanisms that promote adaptations to anthropogenic pressures. The results suggest that (1) two species may infest oil palm plantations in Indonesia: an endemic rat Rattus tiomanicus - which presence is associated with natural habitat typology - and an introduced rats Rattus tanezumi-R3 - which occur in association with the Human Footprint- ; (2) clinal geographic distribution of these species is probably due to both phylogeography and contemporary human activities, and suggest interspecific competition; (3) genetic isolation by distance patterns among these populations, and restricted gene flow potentially influenced by road transport; (4) R. tanezumi-R3 developed a strong physiological resistance to coumatetralyl under AVK exposure. This resistance is not associated with a genetic mutation of the target molecule, and may relate to metabolic enzymes. This work highlights behavioral and physiological adaptations of invasive populations of rodents in agricultural landscape, and thus provides scientific basis for integrated pest management
Article
Worldwide pest rodents on livestock farms are often regulated using anticoagulant rodenticides (ARs). Second generation ARs in particular can cause poisoning in non-target species due to their high toxicity and persistence. However, research on exposure of small mammals is rare. We systematically investigated spatial and temporal exposure patterns of non-target small mammals in a large-scale replicated study. Small mammals were trapped at different distances to bait stations on ten farms before, during and after brodifacoum (BR) bait application, and liver samples of 1178 non-target small mammals were analyzed for residues of eight ARs using liquid chromatography coupled with tandem mass spectrometry. BR residues were present in 23% out of 742 samples collected during and after baiting. We found clear spatial and temporal exposure patterns. High BR residue concentrations mainly occurred within 15 m from bait stations. Occurrence and concentrations of residues significantly decreased with increasing distance. This pattern was found in almost all investigated taxa. After baiting, significantly more individuals contained residues than during baiting but concentrations were considerably lower. Residue occurrence and concentrations differed significantly among taxa, with the highest maximal residue concentrations in Apodemus species, which are protected in Germany. Although Sorex species are known to be insectivorous we regularly found residues in this genus. Residues of active agents other than brodifacoum were rare in all samples. The confirmation of substantial primary exposure in non-target small mammals close to the baiting area indicates considerable risk of secondary poisoning of predators, a pathway that was possibly underestimated until now. Our results will help to develop risk mitigation strategies to reduce risk for non-target small mammals, as well as their predators, in relation to biocidal AR usage.
Conference Paper
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Small mammal population outbreaks are one of the consequences of socio-economic and technological changes in agriculture. They are studied for their economic cost and also for their ecological role in food webs. Here our objective was to study the effect of spatio-temporal changes in crop rotation on the occurrence of the outbreaks of the water vole (Arvicola terrestris) in Haute-Romanche (Alps). Population outbreaks were monitored from 1998 to 2010. Based on plot history (1810-2001), spatio-temporal analysis of crop rotations, and modeling the outbreak wave, our study indicates that water vole population outbreaks in Haute-Romanche are promoted by the presence of grassland corridors increasing hayfield connectivity. They appeared with the virtual disappearance of tilled land and maintaining hayfields.
Article
Second Generation Anticoagulant Rodenticides (SGARs) are currently used for controlling small mammalian pests. Evidences of their negative impact on wildlife have been reported worldwide. In some countries, particularly in Europe, the SGAR bromadiolone is intensively used in the field. It is the only rodenticide authorised in France for controlling the population outbreaks of the Water vole Arvicola terrestris Sherman. Vole control operations using bromadiolone are undertaken over large areas (e.g., hundreds of km²), and dozens to hundreds of secondary poisonings of Red foxes (Vulpes vulpes) have been reported each year. The first aim was to measure bromadiolone persistence in wheat baits and its variability in field conditions. The persistence of bromadiolone in artificial galleries is short (half-life 3-6 days) and weakly influenced by environmental conditions (soil type and climatic conditions). However, this persistence is dramatically increased in baits when they were stored (27< half-life < 45 days). This may cause rodent exposure on a longer duration. The second objective was to assess the kinetic of bromadiolone residues in rodent populations in a treated area. Here, both the Water vole (the target species) and the Common vole Microtus arvalis (a non target species), two rodent species having high density in grassland and both eaten by predators, were studied. Bromadiolone residues in rodent population reached the maximum concentration from the third to the fifth day depending on the species or the tissue and the high concentrations are maintained during 15-20 days. However, the re-colonization in the treated parcel by rodents from the neighbourhood may induce consequences with exposure of rodent until three months after bait distribution. This may explain in part why rodents with bromadiolone residues may be potentially available to predators more than four to six months after a treatment. Finally, we assessed the feasibility of monitoring the exposure of foxes to bromadiolone by analysing the residues in faeces following field treatments. A new LC - MS method was developed. Bromadiolone residues in faeces and blood exhibited similar patterns over time: a dramatic increase during the exposure period (2 or 5 days according to foxes) and then a gradual decrease after the last exposure. Bromadiolone was detected in faeces 15 hours after the first exposure and for at least 24 days after the last exposure (end of the experiment). Two of the foxes presented severe external haemorrhages six days after the first exposure. Their prothrombin time (PT) was multiplied by 6 compared to the day before exposure and they would probably have died without vitamin-K administration. Then, two other studies were achieved in situ. The first demonstrated that 48 % of faeces sampled in an area treated between 15 to 45 days before, contained bromadiolone residues. The second demonstrated an exponential relationship between the rectum content of foxes trapped in an area treated 1 to 6 months before the field surveys, and the residues measured in the liver. These findings provide a basis for programs aiming to monitor the exposure in situ of wild fox populations to bromadiolone using non-invasive methods based on standard sampling and analysis of residues in faeces. After optimisation, it will be possible to determine if different environmental factors may affect fox population exposure without trapping and/or animal death.
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Depuis les années 50, les rodenticides anticoagulants sont couramment utilisés pour contrôler les populations de rongeurs commensaux et de prairie. De nombreux empoisonnements de la faune non cible sont répertoriés partout dans le monde. En Europe de l'Ouest notamment, la bromadiolone est utilisée de façon intensive dans les champs. Elle est le seul rodenticide autorisé en France pour contrôler les populations de Campagnol terrestre, Arvicola terrestris Sherman. Ces opérations utilisant des appâts grains de blé enterrés dans le sol sont réalisées à de larges échelles et des dizaines voire des centaines d'empoisonnements secondaires de prédateurs, dont le renard, sont répertoriés chaque année. Cette étude propose d'apporter des éléments de compréhension sur les modalités de son transfert à travers les systèmes biologiques complexes considérés dans leur intégralité. Le premier objectif a été d'évaluer la variabilité environnementale de la persistance de la bromadiolone dans les appâts en conditions naturelles. Cette persistance dans les galeries de traitement est courte (demi-vie de 3 à 6 jours) et faiblement influencée par les conditions environnementales (type de sol et conditions climatiques). Cependant, elle augmente considérablement lors du stockage des appâts dans des réserves (27<demi-vie<45 jours) et peut constituer un risque d'exposition des rongeurs sur des périodes beaucoup plus longues. Le second objectif a été d'évaluer la cinétique d'intoxication des populations de rongeurs dans les zones traitées avec dans notre cas comme espèce cible, le Campagnol terrestre, et une espèce non cible, le Campagnol des champs Microtus arvalis. Les résidus de bromadiolone dans les deux populations atteignent des concentrations maximales entre 3 et 5 jours après le traitement en fonction de l'espèce ou des tissus et des valeurs élevées sont maintenues pendant 15 à 20 jours. Cependant, la recolonisation de terriers traités peut induire une exposition de rongeurs jusqu'à 3 mois après la distribution des appâts. Ce phénomène permettrait d'expliquer en partie le fait que des rongeurs présentant des résidus de bromadiolone soient disponibles pour des prédateurs plus de 4 à 6 mois après le traitement. Le dernier objectif a été d'évaluer la faisabilité de mesurer, en nature, l'exposition de renards par l'analyse des résidus de bromadiolone dans leurs fèces. Une nouvelle méthode analytique en Chromatographie Liquide et Spectrométrie de Masse a été développée pour les dosages. Les résidus en bromadiolone dans les fèces et dans le plasma de renards captifs nourris pendant cinq jours avec des campagnols intoxiqués montrent des évolutions temporelles similaires : une augmentation rapide pendant la phase d'exposition puis une diminution progressive après celle-ci. La bromadiolone a été détectée dans les fèces dès le premier prélèvement 15 heures après la première exposition et pendant toute la durée de l'expérimentation, i.e., 24 jours après la dernière exposition. La dose administrée (1000 µg broma / j) se serait probablement révélée mortelle pour deux des quatre renards exposés sans l'administration d'antidote. Deux expérimentations ont ensuite été menées en nature. La première a montré que 48% des fèces collectées dans une zone traitée entre 15 et 45 jours auparavant, présentaient des résidus de bromadiolone mesurable. La seconde a montré qu'une relation d'ordre exponentiel reliait les résidus de bromadiolone mesurés dans le foie et ceux mesurés dans les contenus rectaux de renards prélevés dans une zone traitée entre un et six mois auparavant. Ces travaux permettent d'envisager une évaluation indirecte de l'exposition in situ de populations de renards à large échelle spatiale et temporelle. Après l'optimisation de cette méthode de mesure, nous pourrons alors déterminer si différents facteurs environnementaux peuvent moduler cette exposition et cela sans impliquer ni la capture ni la mort de l'animal.
Conference Paper
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The paper reviews the use ot the anticagulant bromadiolone during 18 years in the Jura Mountains, region of Neuchâtel, in attempts to control the outbreaks of fossorial water vole populations (Arvicola terreistris scherman). A large scale treatment over 15,000 ha in 1981-82 caused an unexpected impact on non-target species among which 54 Common buzzards (Buteo buteo),9 Carrion crows (Corvus corones), 5 Red kites (Milvus milvus), 24 Red foxes (Vulpes vulpes), 9 mustelids (Martes sp.), as well as 7 domestic cats and dogs. It was later found that a significant fraction of intoxicated voles left their burrows to die above the ground.
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A method to estimate the abundance of the fossorial form of the water vole Arvicola terrestris scherman (Shaw, 1801) has been developed, by using surface indices. Results are compared to the standard method of estimation using trap lines. These results show quantitatively that it is possible to differentiate reliably mole indices from water vole indices. Moreover, the two species are inclined to exclude each other. Even though water voles share the same galleries as moles, specific surface indices of the water vole occur for any density exceeding 2 ind/trap line (over 20 ind/ha). Several models of abundance estimation are put forward, all of them using linear multiple regressions. Correlations between the estimations from indices and the estimations from trap lines exceed 0.8 and the limits of using abundance classes are tested. Other limits are developed in the discussion. One of them is that the sampling intervals are saturated for densities exceeding 400 ind/ha. The index method, which is easy to carry out, offers the definite advantage of being suitable to space and time scales otherwise incompatible with estimations from trap lines. For instance, it allows distribution maps from wide transects about areas of more than 25 km(2) to be drawn, in less than two days.
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Cereal‐based bait containing 20 ppm brodifacoum was used in bait stations continuously from December 1997 to August 2000 in the Rotoiti Nature Recovery Project area, for controlling brushtail possum (Trichosurus vulpecula), ship rat (Rattus rattus), and house mouse (Mus musculus) populations. Concurrently (and before and after), baits containing brodifacoum, bromadiolone, flocoumafen, coumatetralyl, or warfarin were also used in St Arnaud village and on farms immediately adjacent to the project area. Brodifacoum residues were detected in the livers of 234 mammals from eight species, and two birds from two species captured alive, and a further seven birds from five species found dead in the project area (cause of death unknown). The highest concentration of brodifacoum residues in mammalian livers was recorded during the period brodifacoum was used in the project area. However, residues were present in the livers of some individuals at least 24 months after brodifacoum use in the project area stopped. These residues may have persisted in animals surviving brodifacoum use in the project area, and/or been transported into the area by animals moving to and from the adjacent village and farms, where brodifacoum use continued. Residues of flocoumafen, coumatetralyl, or warfarin, used only in the village and on farms, were also detected in the livers of animals captured up to at least 8 km from the nearest source. The results concur with other studies cautioning against indiscriminate or prolonged use of persistent anticoagulants for vertebrate pest control. However, the risks from such pesticides must be balanced against the demonstrable benefits of reducing pest abundance.
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Ship rats in a North Island podocarp‐hardwood forest were poisoned using brodifacoum in cereal baits presented in bait stations. Livers from 68% of 25 rats captured during and up to three months after poisoning contained brodifacoum residues. Following a rat‐ and possum‐poisoning operation in another podocarp forest, 78% of 40 stoats, 71% of 14 weasels, and 56% of 16 ferrets trapped contained brodifacoum residues. Residue levels in stoats were greater during the three months following the removal of baits than during the poison operation. Female stoats were more likely to contain brodifacoum residues than males, perhaps the result of differences in the dietary habits of the sexes. Brodifacoum was also detected in the livers of the only morepork and in two out of 10 magpies sampled by shooting, but was absent from the livers of four robins, five tomtits, six whiteheads, one bell‐bird, one fantail, one harrier and four red deer. All five pigs and two cats either shot, caught or found dead contained the toxin residues. This study emphasises the potential ecological and human health risks that flow‐on from the use of anticoagulant poisons in New Zealand forests.
Conference Paper
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Anticoagulant rodenticides may pose a secondary poisoning hazard to non-target predators and scavengers because of the time-delay between ingestion of a lethal dose and death of a target rodent. We investigated some pre-lethal effects of an anticoagulant rodenticide on the behavior of wild rats in cages and in enclosures. We found that social interactions shortened time to death, that most rats died away from cover and that thigmotactic behavior was reduced in the enclosures. The normal light-dark rhythm was upset in intoxicated rats in both cages and enclosures. Thus pre-lethal effects are likely to alter the exposure of predators and scavengers to intoxicated rats, and diurnal predators may be exposed more than nocturnal predators as a consequence. We stress the need to extend these behavior studies to the field.
Technical Report
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Anticoagulant pesticides are widely used in New Zealand for vertebrate pest control. The occurrence of residues of the anticoagulant rodenticides brodifacoum, coumatetralyl, warfarin, pindone, and diphacinone in the livers of laboratory rats was measured after they had consumed bait products, under three different bait consumption scenarios for each anticoagulant: at death resulting from presentation of an approximate LD99 amount of anticoagulant bait over 4 days; after 1 day's feeding ad libitum on anticoagulant bait; and at death resulting from ad libitum feeding on a choice of anticoagulant bait and non-toxic pellets. Liver residue concentrations were used as the basis for a conservative assessment of the secondary poisoning risk to non-target predators and scavengers of rodents in New Zealand. Brodifacoum presented the highest overall theoretical risk of secondary poisoning to predators (especially mammals), and a high risk to small and medium scavengers (both birds and mammals). Of the first-generation anticoagulants, diphacinone is likely to present the overall lowest risk of acute secondary poisoning because of its relatively short persistence, a theoretical very low risk to birds, and low to medium risk to mammals. Warfarin has a longer persistence than diphacinone, but also a very low risk profile to birds, and medium risk to mammals. Coumatetralyl is the most persistent of the first-generation compounds, but also has a very low risk profile for birds and a medium risk to mammals. Although pindone has a short persistence similar to diphacinone, it has a high risk profile to birds and a medium risk to mammals. In general, mammals are at greater potential risk of acute secondary anticoagulant poisoning than birds. The efficacy and non-target impacts of diphacinone especially, but also coumatetralyl and warfarin, should be further evaluated as alternative vertebrate pesticides for field uses in New Zealand.
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Eradication of rodent species from some offshore islands has proved to be an effective means of conserving native animal communities and restoring natural ecological processes on the islands. As methods of eradication differ for different rodent species, a truthful monitoring method to detect species presence and relative density is essential for a successful eradication programme. This study compared two spatial arrangements (line vs. grid), 5 different baits (chocolate, cheese, soap, wax, oiled wood) and 3 cover types (transparent plastic, wire netting, galvanised iron) on the detection of 2 species of rodents on Browns (Motukorea) Island in June and August. The two species of rodents present on the island were Norway rats (Rattus norvegicus) and mice (Mus musculus). Trapping using conventional trapping lines and trapping grids was carried out in June and August, respectively. The traps were set for 8 nights for both lines and grids. Trap lines caught 12.40 rats per 100 corrected trap-nights (100 ctn
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We analysed variation in age in a fluctuating population of the common vole ( Microtus arvalis) in southern Moravia, Czech Republic, to test the assumption of the senescence hypothesis that the age of voles increases with increasing population density. Between 1996 and 1998, we monitored the demographic changes by snap-trapping and live-trapping in a field population passing through the increase, peak and decline phase of the population cycle. We used the eye lens mass method to determine the age of snap-trapped animals and those that died in live-traps. The average age of winter males was clearly higher after the peak phase breeding season than before it. No such phase-dependent shift in age, however, was observed in the female component. Male age continued to increase from autumn to spring over the pre-peak winter, and the highest age was in spring of the peak phase year. However, after the peak phase breeding season the highest age was achieved in winter, with the decline phase males during the next spring tending to be younger. The average age of females in spring populations was always lower than in winter populations. The average age of voles from live-traps was always higher than voles from snap-traps, particularly in winter and spring populations, suggesting the presence of senescent animals. Although the density-dependent changes in age are consistent with those observed for other voles, they provide only weak evidence that population cycles in the common vole are accompanied by pronounced shifts in individual age, particularly in female voles.
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Using traps set at regular intervals along drift fences and operated continuously during 100 days, we were able to catch significant numbers of fossorial A. terrestris above the ground. Our observations indicate that young water voles disperse en masse above the ground. Furthermore, these dispersal movements occur mostly during rainy nights. © Société vaudoise des Sciences naturelles Droits de reproduction réservés.
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Brodifacoum was administered to possums at a sub‐lethal dose of 0.1 mg/kg to assess its persistence in blood, muscle, and liver. Only 1 of 68 possums died at this dose level. However, significant increases in one‐stage prothrombin (OSP) and activated partial prothrombin times (APP) confirmed that the possum is susceptible to the anticoagulant effects of brodifacoum. Trace amounts of brodifaooum were detected in plasma for 35 days. Substantial concentrations of brodifacoum were retained in the liver for 8 months. Much lower concentrations were also retained in muscle tissue. The persistence of brodifacoum raises concerns about the possible transfer of this compound through the food chain to humans, dogs, or wildlife.
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A series of toxicological, residue, secondary hazard, and environmental fate studies were completed with bromadiolone. The compound was eliminated rapidly after ingestion by Rattus norvegicus and Mus domesticus. In R. norvegicus, 75% of the bromadiolone was eliminated within 4 days. Dead rodents collected from field trials using bromadiolone had residue levels of 1.92 in R. rattus, 1.17 in M. domesticus, and 0.49 ppm in Spermophilus beecheyi. The LD50 for bromadiolone in beagle dogs was calculated at 8.1 mg kg-1 (10.7 for males and 6.3 mg kg-1 in females). The approximate LD50 in Canis latrans was 10 mg kg-1. Dietary LC50 determination compound in Putorius putorius furo was 9.8 ppm. Secondary hazard studies showed the rodenticide to have little potential to snakes and birds of prey if used properly. Field tests with grain and pelleted baits over 21 days demonstrated that the active ingredient degraded by 78 and 45%, respectively.
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Summary • Monitoring of exposure to pesticides in many countries shows extensive exposure of predators to anticoagulant rodenticides, which are used to control rats. Many predators and scavengers are declining in numbers, and exposure to rodenticides might therefore be of importance in conservation biology. • Predators and scavengers of poisoned rats are at most risk of secondary poisoning. However, several predatory species of conservation concern rarely eat rats, implicating non-target small mammals as the major route of exposure. For the first time, this research investigated the importance of non-target small mammals as routes of exposure to rodenticide for predators and scavengers in the UK. • Exposure studies of non-target small mammals were carried out alongside routine rat control at five sites, around agricultural buildings (n = 2) and feed hoppers for game birds (n = 3). • Three non-target rodent species fed on rodenticide from bait boxes during routine rat control treatments. A large proportion (48·6%) of individuals in local populations ate the bait: woodmice Apodemus sylvaticus were most exposed, followed by bank voles Clethrionomys glareolus then field voles Microtus agrestis. • Local populations of non-target small mammals declined significantly following rodenticidal rat control but their relative proportions did not change significantly. Populations recovered partially after 3 months, depending on the time of the year relative to the breeding cycle. • Synthesis and applications. Our results clearly demonstrate that routine rat control reduced local populations of non-target small mammals. This may limit the food supply of some specialist predators. Most importantly, this demonstrates a significant route of exposure of predators and scavengers of small mammals to secondary poisoning. Rodenticides are applied on farms and game estates across the UK. Hence the results of this study are indicative of non-target rodenticide exposure nationally. Mitigation requires a shift from the current reliance on rodenticides to ecologically based rodent management, involving improvements in site management and the adoption of good farming practice. Journal of Applied Ecology (2005) 42, 118 –128 doi: 10.1111/j.1365-2664.2005.00997.x
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This paper presents the result of a 4 year survey in France (1991-1994) based on the activity of a wildlife disease surveillance network (SAGIR). The purpose of this study was to evaluate the detrimental effects of anticoagulant (Ac) rodenticides in non-target wild animals. Ac poisoning accounted for a very limited number of the identified causes of death (1-3%) in most species. Predators (mainly foxes and buzzards) were potentially exposed to anticoagulant compounds (especially bromadiolone) via contaminated prey in some instances. The liver concentrations of bromadiolone residues were elevated and species-specific diagnostic values were determined. These values were quite similar to those reported in the literature when secondary anticoagulant poisoning was experimentally assessed.
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Determining the relationship between an exposure and the resulting target tissue dose is a critical issue encountered in quantitative risk assessment (QRA). Classical or physiologically based toxicokinetic (PBTK) models can be useful in performing that task. Interest in using these models to improve extrapolations between species, routes, and exposure levels in QRA has therefore grown considerably in recent years. In parallel, PBTK models have become increasingly sophisticated. However, development of a strong statistical foundation to support PBTK model calibration and use has received little attention. There is a critical need for methods that address the uncertainties inherent in toxicokinetic data and the variability in the human populations for which risk predictions are made and to take advantage of a priori information on parameters during the calibration process. Natural solutions to these problems can be found in a Bayesian statistical framework with the help of computational techniques such as Markov chain Monte Carlo methods. Within such a framework, we have developed an approach to toxicokinetic modeling that can be applied to heterogeneous human or animal populations. This approach also expands the possibilities for uncertainty analysis. We present a review of these efforts and other developments in these areas. Appropriate statistical treatment of uncertainty and variability within the modeling process will increase confidence in model results and ultimately contribute to an improved scientific basis for the estimation of occupational and environmental health risks.
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The risks to non-target birds and other wildlife from the use of vertebrate pesticides, including anticoagulant rodenticides, are determined to a significant extent by species' intrinsic susceptibility, and the toxicokinetics of the compounds used. Brodifacoum is highly toxic to birds and mammals. The acute toxicity of brodifacoum to birds in New Zealand varies from <1 mg/kg in pukeko (Porphyrio p. melanotus), the native swamp hen, to >20 mg/kg in the paradise shelduck (Tadorna variegata). Like other second-generation anticoagulants brodifacoum is strongly bound to vitamin K epoxide reductase and will persist, apparently for at least 6 months, in organs and tissue containing this enzyme, e.g., liver, kidney, and pancreas. The unique toxicokinetics of this class of compound exacerbates the risk of primary and secondary poisoning of non-target species. Vertebrate pest control programmes in New Zealand using bait containing brodifacoum have resulted in the primary and secondary poisoning and sub-lethal contamination of non-target species. These include native raptors, such as the Australasian harrier (Circus approximans) and morepork (Ninox novaeseelandiae), other native birds such as the pukeko, weka (Gallirallus australis), southern black-backed gull (Larus dominicanus), and kiwi (Apteryx spp.), and introduced mammals, including game animals. There are increasing numbers of reports worldwide of wildlife contamination and toxicosis after the use of second-generation anticoagulants. All pest control activities require careful risk-benefit assessment in view of their potential to cause adverse environmental impact. Monitoring of wildlife for pesticide residues will provide data that can be used to reduce the risk of anticoagulant bioaccumulation and mortality in non-target species.
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Because of the rapid decline of the endangered European mink (Mustela lutreola) populations in France, a national conservation program has been put into action, including research to understand the causes of decline. As part of this research, concentrations of eight anticoagulant rodenticides were examined in livers from 122 carcasses of four species of free-ranging mustelids collected between 1990 and 2002 in southwestern France. Bromadiolone residue was found in all species and 9% of the sample (one of 31 European mink, three of 47 American mink [Mustela vison], five of 33 polecats [Mustela putorius], and two of 11 European otters [Lutra lutra]). Liver concentrations ranged from 0.6 mug/g to 9.0 mug/g. Chlorophacinone residue was found in two species and 4% of the sample (in four of the American mink and in one of the otters), with liver concentrations ranging from 3.4 mug/g to 8.5 mug/g. Two polecats and one American mink had lesions and liver residues indicating bromadiolone was directly responsible for their death. However, most of our study animals survived secondary poisoning until they were caught; this study certainly underestimates the extent of fatal exposure of mustelids to rodenticides. Moreover, anticoagulant poisoning could increase their vulnerability to other causes of death. The current status of the endangered European mink population is such that any additional risk factor for mortality is important, and it is thus urgent to monitor and reduce the extensive use of bromadiolone and chlorophacinone against field rodents in France.
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To assess the rate and extent of ruminal degradation of warfarin, chlorophacinone, and bromadiolone in vitro and determine the oral availability and clinical and hemostatic effects of each anticoagulant rodenticide in adult sheep. 3 Texel sheep. Samples of ruminal fluid were incubated with each of the anticoagulants to assess the kinetics of ruminal degradation over 24 hours. To determine the plasma kinetics of the anticoagulants, each sheep received each of the anticoagulants IV or via a rumenimplanted cannula at 2-month intervals (3 rodenticide exposures/sheep). At intervals during a 240- to 360- hour period after treatment, prothrombin time (PT) was measured, plasma anticoagulant concentration was assessed, and clinical signs of rodenticide poisoning were monitored. In plasma and rumen extracts, anticoagulant concentrations were determined via high-performance liquid chromatography. In the rumen extracts, anticoagulants were slightly degraded (< 15%) over 24 hours. In vivo, oral availability of warfarin, chlorophacinone, and bromadiolone was estimated at 79%, 92%, and 88%, respectively. Although maximum PT was 80 seconds after chlorophacinone and bromadiolone treatments, no clinical signs of toxicosis were detected; PT returned to baseline values within 2 weeks. In sheep, warfarin, chlorophacinone, and bromadiolone were not degraded in the rumen but their bioavailabilities were high after oral administration; the kinetics of these compounds in sheep and other mammals are quite similar. These data suggest that the lack of susceptibility of ruminants to these anticoagulant rodenticides cannot be explained by either ruminal degradation or the specific toxicokinetics of these anticoagulants.
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Pesticides are widely used to control agricultural pests. Unfortunately, because of their biological activity, they may have detrimental effects on nontarget species. Acute toxicity, resulting in death, is reported worldwide. Although chronic and indirect effects may be even more hazardous for animal populations on a long-term basis, they are usually evaluated as parts of research programs. The purpose of this paper was to review the wildlife-poisoning surveillance systems and their results regarding the circumstances of exposure of wild animals, the pesticides involved and the species exposed. Most data are retrieved from the British and French pesticide poisoning surveillance systems in wildlife, with some data from other European structures.
Article
Some complexities and limitations of using carcass residue data to determine secondary hazard to nontarget species are discussed. The roles of chemical and toxicological properties of the rodenticide such as metabolism, excretion, organs of retention, site of absorption and latent period in secondary hazard are reviewed and examples given. The possible effects of bait composition and application methods, the behavioral response of the nontarget species, and local environmental factors upon secondary hazard are outlined.
Article
From 1971 through 1997, the authors documented 51 cases (55 individual animals) of poisoning of nontarget wildlife in New York (plus two cases in adjoining states) (U. S. A) with anticoagulant rodenticides-all but two of these cases occurred in the last eight years. Brodifacoum was implicated in 80 percent of the incidents. Diphacinone was identified in four cases, bromadiolone in three cases (once in combination with brodifacoum), and chlorophacinone and coumatetralyl were detected once each in the company of brodifacoum. Warfarin accounted for the three cases documented prior to 1989, and one case involving a bald eagle (Haliaeetus leucocephalus) in 1995. Secondary intoxication of raptors, principally great horned owls (Bubo virginianus) and red-tailed hawks (Buteo jamaicensis), comprised one-half of the cases. Gray squirrels (Sciurus carolinensis), raccoons (Procyon lotor), and white-tailed deer (Odocoileus virginianus) were the most frequently poisoned mammals. All of the deer originated from a rather unique situation on a barrier island off southern Long Island (NewYork, U. S. A.). Restrictions on the use of brodifacoum appear warranted.
Article
In Britain, the use of "second-generation" rodenticides has become widespread on agricultural premises. The high toxicity and relatively long half-lives of these compounds has raised concerns over potential secondary exposure and poisoning of non-target predators. Over the last 15 years, exposure has been extensively documented in the barn owl Tyto alba but relatively little is known about mammalian terrestrial predators. This paper reviews recent studies and demonstrates that there is evidence of both secondary exposure and secondary poisoning in a variety of non-target, terrestrial mammals in Britain. It also presents new data on rodenticide levels in the polecat Mustela putorius which preys on farmyard rats in winter in Britain and is, therefore, considered to be highly vulnerable to exposure to rodenticides. The new data demonstrated that 26% of polecats in the sample contained difenacoum or bromadiolone and that exposure was geographically widespread and occurred in several years. The possible effects of secondary exposure on populations of polecats and other predators are discussed.
Article
Stoat (Mustela erminea) density was estimated by live-trapping in a South Island Nothofagus forest, New Zealand, at 8-9 (Jan/Feb 1996) and 15-16 (Aug/Sep 1996) month intervals after significant beech seedfall in autumn 1995. Absolute densities were 4.2 stoats km-2 (2.9-7.7 stoats km-2, 95% confidence intervals) in Jan/Feb 1996 and 2.5 stoats km-2 (2.1-3.5 stoats km-2) in Aug/Sep 1996. Trappability of stoats increased in the latter sampling period, probably because mice (Mus musculus) had become extremely scarce. Accordingly, trapping rates of stoats may vary temporally and spatially with food supply rather than only with absolute abundance. Ship rats (Rattus rattus) capture rates doubled between Jan/Feb 1996 and Aug/Sep 1996, but rapidly declined shortly afterwards. Trappability of ship rats also increased in the latter sampling period. These factors must be considered when planning methods of indexing relative densities of stoats and rats.
Article
This study investigates the effect of land use, and landscape composition and structure on the population dynamics of fossorial water vole (Arvicola terrestris scherman Shaw). Water vole populations were monitored from 1989 to 1994 in the Doubs department, France, by using index methods. Land use patterns were studied based on agriculture and forestry data from the French Ministry of Agriculture collected in 1956, 1970, 1979 and 1988. Grassland quality and landscape structure were studied based on field transects, combined with the assessment of landscape structure from maps at 1:25,000 scale. Outbreaks of water vole populations occurred as a wave, spreading from epicentres over more than 2500 km2. The propagation speed was in excess of 10 km/yr. On a regional level (n × 10 km) and over 5 years and more, density variation patterns of water vole were linked to the ratio of ploughed land and of permanent grassland to farmland. At a sectional scale (n × 1 km), forests and uncultivated lands had a dampening effect both on the outbreaks and on their duration. The evolution of farmlands from 1956 to 1988 was apparently the major cause of increase in density variations of water vole. Therefore, land use and landscape management could be a way to control water vole outbreaks, and their effects are discussed.
Article
Les pullulations de certaines espèces de rongeurs champêtres rendent nécessaire une lutte destinée à protéger des cultures; dans le cas du campagnol terrestre (Arvicola terrestris scherman) et des dommages aux prairies de montagne, celle-ci se fait au moyen ďun appât ‘carottes en rondelles enrobées ďun concentrat de bromadiolone’ titrant 100 ppm de matière active pour la France, et ďun appât sec titrant 140 ppm pour la Suisse. Nous avons churchéàévaluer expérimentalement le risque découlant de ľutilisation de cet anticoagulant pour les prédateurs du campagnol terrestre, en choisissant comme modèles ľhermine (Mustela erminea) et la buse variable (Buteo buteo). Les campagnols terrestres, consommant de ľappât carottes durant 24 h et sacrifiés aussitôt, contenaient 6,5-6,75 ppm de bromadiolone; ceux ayant consommé le même appât carottes durant 3 j consécutifs et sacrifiés à la fin du 3e j, en contenaient 8,72–10,93 ppm, tandis que ceux ayant consommé de ľappât sec, dans les mêmes conditions, n'en contenaient que 5,81 ppm (mais cet appât sec s'est révélé ne titrer que 102,5 ppm au lieu des 140 ppm théoriques). Si les campagnols ayant consommé durant 1 ou 3 j étaient sacrifiés 2 j après la dernière intoxication, le niveau des résidus était divisé, respectivement, par 4 et 9, tombant au-dessous de 2 ppm. Chez les hermines (14 individus) consommant des campagnols intoxiqués durant 1 j, la mortalité est apparue (1/3) au bout de 5 j ďingestion; cependant, les survivantes ont été malades, même celles n'ayant subi que 3 j ďingestion. Chez les buses variables (108 individus), la mortalité n'est apparue que s'il y a eu répétition des ingestions durant 3 j consécutifs, que les campagnols aient eux-mêmes été intoxiqués durant 1 ou 3 j ou, si après 1 ingestion et 10 j de nourriture normale, ces buses ont été soumises à une seconde intoxication unique. Le foie était bien ľorgane de stockage des résidus, chez les deux espèces de prédateurs, les reins en contenant presque exclusivement chez des animaux sacrifiés 24 h après intoxication ou ceux morts dans de courts délais. Une grande variabilité interindividuelle a été constatée. Le risque ďintoxication pour ces deux espèces de prédateurs, en fonction de la technique française de lutte contre le campagnol terrestre, semble peu élevé.
Article
Predation on the fossorial form of the water volc by the red fox was studied in western Switzerland from April 1988 to February 1991. As well as analysis of the ramains found in fox scats collected monthly, seasonal trapping was carried out to estimate water vole density. During this study, the water vole was the main prey of the fox, representing 54.5% of all items (n=1707). There was a significant correlation between availability of water voels and their consumption by the red fox.