Determinants of exposure to veterinary pharmaceuticals in avian scavengers to improve environmental risk assessment

Abstract

Pharmaceuticals are considered emerging contaminants. These compounds are increasing worldwide and their presence in the environment is now ubiquitous. Their negative impacts on biota are an increasing concern globally. The clearest example of this has been the dramatic decline in Asian vulture populations in recent decades, driven primarily by the non-steroidal anti-inflammatory drug (NSAID) diclofenac. This caused acute intoxication in Gyps vultures when they consumed carcasses of previously treated livestock. This well-known NSAID was then subsequently authorized for veterinary use in Spain in 2013, which was highly controversial given Spain is an important stronghold for European vulture conservation. In this context, this thesis focused on the description and analyses of parallel scenarios in Spain regarding veterinary pharmaceuticals and their potential negative effects in wildlife with scavenging habits (mainly vultures). This thesis describes the prevalence of highly toxic compounds (like NSAIDs and barbiturates) to avian scavengers in Spain, but also considers other commonly used veterinary pharmaceuticals like antibiotics or antiparasitic drugs. Data are reported here for avian scavenger samples and for their main source of exposure, livestock carcasses supplied at feeding stations. Using these data, we determined risk factors for exposure to pharmaceuticals that are associated with livestock carcasses supplied for avian scavengers in Spain. To accomplish these objectives, various analytical methods were developed to detect veterinary pharmaceuticals in samples using liquid and gas chromatography coupled to mass spectrometry. This included a ‘final’ multiresidue method to analyse up to 49 pharmaceuticals commercialized for veterinary use in Spain. The prevalence of different NSAIDs detected here ranged between 0.3-14.3% in avian scavengers (in plasma and tissues) and between 0.6-4.4% in domestic animal carcasses. Barbiturates were found in 3.4% of wildlife tissues analysed, with avian scavengers showing barbiturate residues in 2.7% of samples collected. For antibiotics, prevalence among the different compounds detected ranged between 0.3-13.1% in avian scavengers and between 0.6-17.6% in livestock carcasses, while antiparasitic drugs (like avermectins) were not detected. Considering the levels found here, we estimated that in most cases the carcasses supplied for avian scavengers contained low concentrations that would probably not cause mortality in vultures feeding on them. However, we must highlight that some carcasses had potentially toxic levels of flunixin and two pig carcasses contained diclofenac, one at toxic levels. This thesis also contains a description of the first case of a cinereous vulture dying due to diclofenac poisoning in Europe, which highlights the risk of this for avian scavengers. We also report on intoxications with other highly toxic pharmaceuticals like NSAIDs (i.e., flunixin) and pentobarbital. In the case of the latter, we note a worrying increase in the incidence of poisoning events (mainly in the north of Spain). Together with the pharmaceuticals described here, caffeine was observed in plasma from a big proportion of avian scavengers (64.1%) for the first time. We noted caffeine may be a good biomarker for landfill use by vultures. This thesis contributes to knowledge regarding the ecotoxicology of pharmaceuticals in avian scavengers in Spain. This is a fundamental starting point to establish research needs and to perform adequate risk assessments for these compounds in wildlife. This thesis also includes general recommendations for decision makers to improve the management of domestic animal carcasses in terms of preventing exposure to pharmaceuticals in wildlife.