Increased rodenticide exposure rate and risk of toxicosis in barn owls (Tyto alba) from southwestern Canada and linkage with demographic but not genetic factors

Abstract

Among many anthropogenic drivers of population decline, continual rapid urbanization and industrialization pose major challenges for the survival of wildlife species. Barn owls (Tyto alba) in southwestern British Columbia (BC) face a multitude of threats ranging from habitat fragmentation to vehicle strikes. They are also at risk from secondary poisoning of second-generation anticoagulant rodenticides (SGARs), a suite of toxic compounds which at high doses results in a depletion of blood clotting factors leading to internal bleeding and death. Here, using long-term data (N = 119) for the hepatic residue levels of SGAR, we assessed the risk of toxicosis from SGAR for the BC barn owl population over the past two decades. We also investigated whether sensitivity to SGAR is associated with genetic factors, namely Single Nucleotide Polymorphisms (SNPs) found in the CYP2C45 gene of barn owls. We found that residue concentration for total SGAR was significantly higher in 2006-2013 (141 ng/g) relative to 1992-2003 (57 ng/g). The proportion of owls exposed to multiple SGAR types was also significantly higher in 2006-2013. Those measures accordingly translate directly into an increase in toxicosis risk level. We also detected demographic differences, where adult females showed on average lower concentration of total SGAR (64 ng/g) when compared to adult males (106 ng/g). Juveniles were overall more likely to show signs of toxicosis than adults (33.3 and 6.9 %, respectively), and those symptoms were positively predicted by SGAR concentrations. We found no evidence that SNPs in the CYP2C45 gene of barn owls were associated with intraspecific variation in SGAR sensitivity. We recommend several preventative measures be taken to minimize wildlife exposure to SGAR.

Challenges in the interpretation of anticoagulant rodenticide residues and toxicity in predatory and scavenging birds

“…This is likely due to greater demand for pest control services related to increased rodent populations, 9 although adoption of more sensitive analytical methods (shift from high‐performance liquid chromatography ultraviolet/fluorescence to liquid chromatography‐mass spectrometry/tandem mass spectrometry) may also be a contributing factor to this trend 11 . Similar temporal trends have been observed for the red kite ( Milvus milvus ) in Britain 12–15 and for the barn owl ( Tyto alba ) in Britain 16,17 and Canada 18 . With evidence of multiple AR exposure in birds, the summing of residue concentrations of various ARs detected in the liver of an individual bird has become commonplace for investigators examining spatial and temporal trends, and for diagnosticians attempting to determine cause of death in postmortem evaluations (see Table S1).…”

Continued Anticoagulant Rodenticide Exposure of Red‐tailed Hawks (Buteo jamaicensis) in the Northeastern United States with an Evaluation of Serum for Biomonitoring

“…In addition, the first survey of ARs in wildlife in Finland, which was conducted after the implementation of AR regulatory measures in that country in 2011, found residues in 82% of 17 species of avian and mammalian predators and scavengers (Koivisto et al 2018). As different countries implement overlapping and divergent risk‐mitigation strategies, continued data‐driven evaluation of the effectiveness of these measures through analysis of temporal trends in sentinel species is critical (Huang et al 2016; Buckle and Prescott 2018; Eisemann et al 2018; Lohr and Davis 2018; Sainsbury et al 2018).…”

“…For example, AR exposure in a species protected under the US Federal Endangered Species Act, the northern spotted owl ( Strix occidentalis caurina ), has been documented in 7 out of 10 opportunistically collected liver samples in California, USA (Gabriel et al 2018). Other examples of AR exposure in birds of prey of conservation concern occur worldwide (Huang et al 2016; Coeurdassier et al 2019). Studies have evaluated blood coagulation testing as a means of assessing exposure to ARs antemortem (Webster et al 2015; Hindmarch et al 2019).…”

The potential of VKORC1 polymorphisms in Mustelidae for evolving anticoagulant resistance through selection along the food chain

“…dicoumarol [8,9]), coumarin derivatives such as warfarin have been developed to lower blood coagulation and clogging for both therapeutic applications [10,11] and rodent control [12,13]. Metabolized coumarin derivatives affect blood coagulation in vertebrates by inhibition of the vitamin K epoxide reductase complex subunit 1 (VKORC1) [14,15,16], a small transmembrane protein of the endoplasmic reticulum of most eukaryotes [17,18]. It recycles vitamin K 2,3-epoxide to vitamin K hydroquinone, which is essential for the posttranslational γ-carboxylation of many blood coagulation factors [17].…”