Bone Density and Breaking Strength in UK Raptors Exposed to Second Generation Anticoagulant Rodenticides

Abstract

Second generation anticoagulant rodenticides (SGARs) such as difenacoum, brodifacoum, and bromadiolone are more persistent and acutely toxic than their first generation counterparts (such as warfarin), and are designed to deliver a lethal dose during a single feeding (US EPA 2004). These properties make SGARs effective primary rodenticides and they have become extremely important for rodent control worldwide. However, their high acute toxicity and relatively long tissue half-lives present the potential for secondary exposure in predatory birds and mammals that feed upon exposed rodents. Mortality incidents have been documented amongst non-target predators but, perhaps more striking yet is the wide-scale (large proportions of each population, multiple species) exposure (Stone et al. 1999; Howald et al. 1999; Eason et al. 2002; Shore et al. 2006). There is considerable concern that this widespread and large-scale ‘sub-lethal’ exposure (or at least, exposure not visibly associated with hemorrhagic symptoms) may potentially be associated with other adverse effects. SGARs elicit their acute toxicity by inhibiting the synthesis of vitamin K, which leads to increased coagulation times followed by lethal internal hemorrhage (US EPA, 2004). However, vitamin K also plays a role in bone metabolism as it is required for the formation of c-carboxyglutamyl, a component of bone proteins such as osteocalcin (Weber 2001). Studies on humans have shown that warfarin therapy and low dietary vitamin K intake are related to reduced bone density, increased frequency of bone fractures and osteoporosis (Barnes et al. 2005). Given this, we tested the hypothesis that wild birds exposed to periodic sub-lethal concentrations of SGARs may also exhibit decreased bone density and bone strength, possibly placing them at risk for bone fractures.