Science of the Total Environment 731 (2020) 139198 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Review Towards harmonisation of chemical monitoring using avian apex predators: Identification of key species for pan-European biomonitoring Alexander Badry a,⁎, Oliver Krone a, Veerle L.B. Jaspers b, Rafael Mateo c, Antonio García-Fernández d, Madis Leivits e, Richard F. Shore f a Leibniz Institute for Zoo and Wildlife Research, Department of Wildlife Diseases, Alfred-Kowalke-Straße 17, 10315 Berlin, Germany b Department of Biology, Norwegian University of Science and Technology, Høgskoleringen 5, 7491 Trondheim, Norway c Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC, UCLM, JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain d Toxicology and Risk Assessment Group, Department of Health Sciences, University of Murcia, Espinardo Campus, 30100 Murcia, Spain e Chair of Clinical Veterinary Medicine, Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Kreutzwaldi 62, 51006 Tartu, Estonia f UK Centre for Ecology and Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg LA1 4AP, UK HIGHLIGHTS GRAPHICAL ABSTRACT • We identified key raptor and owl spe- cies for pan-European monitoring of pollutants. • Selection was primarily on key ecologi- cal traits and distribution. • Our focus was on Pb, Hg, rodenticides, pesticides and veterinary medicinal products. • Common buzzard and tawny owl were the most suitable pan-European biomonitors. article info abstract Article history: Biomonitoring in raptors can be used to study long-term and large-scale changes in environmental pollution. In Received 19 February 2020 Europe, such monitoring is needed to assess environmental risks and outcomes of chemicals regulation, which is Received in revised form 1 May 2020 harmonised across the European Union. To be effective, the most appropriate sentinels need to be monitored. Our Accepted 1 May 2020 aim was to identify which European raptor species are the likely most appropriate biomonitors when pollutant Available online 07 May 2020 quantification is based on analysing tissues. Our current study was restricted to terrestrial exposure pathways Editor: Adrian Covaci and considered four priority pollutant groups: toxic metals (lead and mercury), anticoagulant rodenticides, pes- ticides and medicinal products. We evaluated information on the distribution and key ecological traits (food web, Keywords: foraging trait, diet, preferred habitat, and migratory behaviour) of European raptors to identify the most appro- Pan-European monitoring priate sentinel species. Common buzzard (Buteo buteo) and/or tawny owl (Strix aluco) proved the most suitable Pollutants candidates for many of the pollutants considered. Moreover, they are abundant in Europe, enhancing the likeli- Pesticides hood that samples can be collected. However, other species may be better sentinels for certain pollutants, such as Metals the golden eagle (Aquila chrysaetos) for lead, the northern goshawk (Accipiter gentilis)formercuryacrossareas Rodenticides including Northern Europe, and vultures (where they occur in Europe) are likely best suited for monitoring Raptors non-steroidal anti-inflammatory drugs (NSAIDs). Overall, however, we argue the selection of candidate species ⁎ Corresponding author. E-mail address: [email protected] (A. Badry). https://doi.org/10.1016/j.scitotenv.2020.139198 0048-9697/© 2020 Published by Elsevier B.V. 2 A. Badry et al. / Science of the Total Environment 731 (2020) 139198 for widescale monitoring of a range of pollutants can be reduced to very few raptor species. We recommend that the common buzzard and tawny owl should be the initial focus of any pan-European raptor monitoring. The lack of previous widespread monitoring using these species suggests that their utility as sentinels for environmnetal pollution has not been widely recognised. Finally, although the current study focussed on Europe, our trait-based approach for identifying raptor biomonitors can be applied to other continents and contaminants. © 2020 Published by Elsevier B.V. Contents 1. Birdsofpreyassentinelsforpollutionmonitoring.............................................. 2 2. Prioritisedenvironmentalpollutants.................................................... 2 3. Methodsofselectionofcandidatespeciesbasedonecologicaltraits...................................... 3 4. CandidatespeciesforbiomonitoringofprioritisedenvironmentalpollutantswithinEurope............................5 4.1. Tracemetals............................................................ 5 4.1.1. Lead(Pb)......................................................... 5 4.1.2. Mercury(Hg)....................................................... 6 4.2. Anticoagulantrodenticides(ARs)................................................... 7 4.3. Pesticides............................................................. 9 4.4. Medicinalproducts(MPs)...................................................... 9 5. Conclusions................................................................10 Funding....................................................................11 Acknowledgements..............................................................11 AppendixA. Supplementarydata........................................................11 References...................................................................11 1. Birds of prey as sentinels for pollution monitoring capability, such as EURAPMON; www.eurapmon.net and its follow-up programme, the European Raptor Biomonitoring Facility ERBFacility; The monitoring of environmental pollutants in raptors has a long www.erbfacility.eu (Movalli et al., 2019). However, a key challenge for history (Cade et al., 1971; Helander et al., 1982; Ratcliffe, 1967). Such large-scale monitoring is to determine which species, or guild of species, monitoring was often initiated to understand the risks from pollutants are likely to be the most suitable sentinels for monitoring contaminants to individual species of high conservation value, but it is now recognised and how species selection may vary depending upon the contaminants that it also can provide insights into wider ecological health and a warn- of interest. This is a critical knowledge gap. ing of potential human exposure and effects on health (García- The current study aimed to address this gap and evaluate the relative Fernández et al., 2020). There are a number of characteristics that merits and disadvantages of different species for harmonised biomoni- make predatory birds particularly suitable as sentinels, especially for toring within and across large-spatial scales such as Europe. We compounds that bioaccumulate or biomagnify through food webs. shortlisted candidate species based on their European distribution and These include foraging through both terrestrial and aquatic food webs, on ecological traits relevant to exposure to priority environmental pol- occupation of high trophic position (typically raptors are apex preda- lutants. Our initial analysis indicated that the distribution across tors), a long history of ecotoxicological research and associated under- Europe of raptors that utilise aquatic food-webs was largely limited standing of contamination in various species, and, where appropriate, and it is arguable that non-raptor and non-avian species, such as the the potential to obtain non-destructive samples (feathers, carcasses Eurasian otter (Lutra lutra), gull species and pinnipeds, may prove from accidents, deserted eggs, blood) for analysis (Espín et al., 2016; more suitable for large-scale biomonitoring of pollutant transfer Gómez-Ramírez et al., 2014). through freshwater and marine systems. Therefore, the present work Monitoring in raptors can reveal spatio-temporal trends in environ- focuses on terrestrial exposures to priority pollutants. Our work builds mental contaminant concentrations (Gómez-Ramírez et al., 2019; on previous research into monitoring schemes that were, or currently López-Perea and Mateo, 2018; Walker et al., 2012). It can therefore be are, operative within Europe (Gómez-Ramírez et al., 2014) and the a key tool for evaluating the outcomes of regulation and other mitiga- practicalities of what sample types are suitable for pollution studies tion measures designed to reduce environmental contamination over (Espín et al., 2016). large spatial scales (García-Fernández, 2020; Shore and Taggart, 2019). Monitoring at national or smaller spatial scales across Europe 2. Prioritised environmental pollutants has involved the use of a variety of species (Gómez-Ramírez et al., 2014) and sample types (Espín et al., 2016). However, chemical regula- We focussed on addressing which species may be most suitable for tion in much of Europe is now harmonised and delivered through monitoring a sub-set of priority compounds. The choice of compounds European Union (EU) directives and regulations, such as the Biocidal was agreed at a European workshop of 30 experts that was hosted by Product Regulation (EU 528/2012), regulation on Plant Protection Prod- the ERBFacility in February 2019. Pollutants were selected on the basis ucts (EC 107/2009) and REACH - Registration, Evaluation, Authorisation that they remain a current environmental risk across Europe, particu- and Restriction of Chemicals (EC 1907/2006). Recently, the European larly to vertebrate wildlife, and are typically also subject to regulation. Parliament