Primary Exposure and Effects in Non-target Animals

Abstract

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 nontarget 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.

Is Sensitivity to Anticoagulant Rodenticides Affected by Repeated Exposure in Hawks?

“…Using hematocrit and blood clotting times as endpoints, dietary exposure of captive kestrels to environmentally realistic concentrations (Merson et al 1984, Primus et al 2001, Ramey et al 2007, Vyas et al 2012, Pitt et al 2015, Shore and Coeurdassier 2018 of the FGAR chlorophacinone or the SGAR brodifacoum did not affect sensitivity to a subsequent low-level dietary dose of chlorophacinone. Based upon previous studies in kestrels (Rattner et al 2015), a seven-day, no-choice dietary exposure to 1.5 µg chlorophacinone/g-ww or to 0.5 µg brodifacoum/g ww evokes coagulopathy and results in substantial hepatic residues of these ARs.…”

“…The concentrations of BROD and CPN in these test diets are believed to be environmentally realistic for rodent prey in proximity to AR control activities. For example, nominal concentration of brodifacoum in the kestrel test diet was 0.5 µg/g ww; average carcass concentrations in target meadow voles (Microtus pinorum) and black rats (Rattus rattus) following field control and eradication activities were reported to be 0.35 and 3.75 µg/g ww, respectively (Merson et al 1984, Pitt et al 2015, and estimated whole body concentrations in several species non-target small mammals range from 0.3 to 3.6 µg/g ww (reviewed in Shore and Coeurdassier 2018). Likewise, nominal concentrations of CPN in kestrel test diets were 0.25 and 1.5 µg/g ww, and were within the range of concentrations detected in carcasses of Belding's ground squirrels (Spermophilus beldingi), pocket gophers (Thomomys bottae), and voles (Microtus spp.)…”

“…A complicating factor is that several of these values (Primus et al 2001, Ramey et al 2007, Pitt et al 2015 were derived carcass samples from which liver was removed, and may underestimate potential exposure. Brodifacoum and chlorophacinone residue concentrations in prey liver can be much greater than in prey carcass (e.g., Vyas et al 2012, Shore andCoeurdassier 2018). Hawk species, for which the kestrel may be the most appropriate model, do not ingest entire mammalian prey, but selectively feed on liver, muscle and some organs.…”

Brodifacoum Toxicity in American Kestrels (Falco sparverius) with Evidence of Increased Hazard on Subsequent Anticoagulant Rodenticide Exposure

“…Concentrations of brodifacoum and chlorophacinone in test diets are believed to be environmentally realistic for rodent prey foraging in proximity to AR control and eradication activities. For example, nominal concentrations of brodifacoum in test diets ranged from 0.3 to 3.0 µg/g wet weight; average carcass concentrations in target meadow voles ( Microtus pennsylvanicus ) and black rats ( Rattus rattus ) following field control and eradication activities have been reported to be 0.35 and 3.75 µg/g wet weight, respectively (Merson et al ; Pitt et al ), and estimated whole‐body concentrations in several species of nontarget small mammals range from 0.3 to 3.6 µg/g wet weight (Shore and Coeurdassier ). Similarly, nominal concentrations of chlorophacinone in test diets were 0.75 and 1.5 µg/g wet weight, which fall within the range (0.131–1.59 µg/g wet wt) detected in carcasses of Belding's ground squirrels ( Spermophilus beldingi ), pocket gophers ( Thomomys bottae ), and voles ( Microtus spp.)…”

Monitoring Anticoagulant Rodenticides in Birds of Prey in the Wildlife Rehabilitation Setting

“…Firstly, while exposure to ARs among birds of prey has been shown to be widespread (Stone et al 2003, Berny and Gaillet 2008, Albert et al 2010, Murray 2011, Stansley et al 2014, Murray 2017, there is little knowledge about the route through the food chain ARs take to reach these secondary consumers. Residues of ARs have been documented in both target rodents and nontarget mammals, as well as in songbirds and invertebrates , Alomar et al 2018, Shore and Coeurdassier 2018. Wildlife rehabilitation-based studies are not able to determine the prey through which secondary exposure occurs due to the delay between ingestion and the manifestation of signs of toxicosis.…”