A review of constraints and solutions for collecting raptor samples and contextual data for a European Raptor Biomonitoring Facility.

The COST Action 'European Raptor Biomonitoring Facility' (ERBFacility) aims to develop pan-European raptor biomonitoring in support of better chemicals management in Europe, using raptors as sentinel species. This presents a significant challenge involving a range of constraints that must be identified and addressed. The aims of this study were to: (1) carry out a comprehensive review of the constraints that may limit the gathering in the field of raptor samples and contextual data, and assess their relative importance across Europe; and (2) identify and discuss possible solutions to the key constraints that were identified. We applied a participatory approach to identify constraints and to discuss feasible solutions. Thirty-one constraints were identified, which were divided into four categories: legal, methodological, spatial coverage, and skills constraints. To assess the importance of the constraints and their possible solutions, we collected information through scientific workshops and by distributing a questionnaire to stakeholders in all the countries involved in ERBFacility. We obtained 74 answers to the questionnaire, from 24 of the 39 COST participating countries. The most important constraints identified were related to the collection of complex contextual data about sources of contamination, and the low number of existing raptor population national/regional monitoring schemes and ecological studies that could provide raptor samples. Legal constraints, such as permits to allow the collection of invasive samples, and skills constraints, such as the lack of expertise to practice necropsies, were also highlighted. Here, we present solutions for all the constraints identified, thus suggesting the feasibility of establishing a long-term European Raptor Sampling Programme as a key element of the planned European Raptor Biomonitoring Facility.

Annual abundance of common Kestrels (Falco tinnunculus) is negatively associated with second generation anticoagulant rodenticides.

Rats and mice can damage food and agricultural products as well as transmit diseases, thereby requiring control of their numbers. Application of Second Generation Anticoagulant Rodenticides (SGARs) often reduces rodent numbers locally. However, predators eating rodents, including non-target species, that have consumed SGARs may be secondarily exposed and potentially lethally poisoned. Here we study whether SGARs may have contributed to the widespread population declines of a rodent-eating raptor, the Common Kestrel (Falco tinnunculus) in the UK. We show that 161 (66.8%) of the 241 Kestrels submitted for ecotoxicology tests between 1997 and 2012 had detectable levels of at least one SGAR in their livers. Adult Kestrels had significantly higher prevalence of SGARs than juveniles, suggesting accumulation of SGARs through time. The prevalence and concentrations of individual SGARs in Kestrels were significantly higher in England than in Scotland. SGAR prevalence in Kestrels were positively associated with some land cover types, primarily arable cereals and broad-leaved woodland, and negatively associated with mainly mean elevation, probably reflecting variation in SGAR usage across land cover types. By using volunteer-collected data on national Kestrel abundance 1997-2012, we show that there is a negative correlation between the Kestrel population index in a specific year and the concentration of bromadialone as well as the total SGAR concentration in the same year. Although correlative, this is the first study to provide evidence for a potential population-limiting effect of SGARs on a raptor.

Decabromodiphenylether trends in the European environment: Bird eggs, sewage sludge and surficial sediments.

Concern on relatively high levels and the potential bioaccumulation of decabromodiphenylether (BDE209) has led to a European 8-year monitoring program on trends in BDE209 concentrations in birds, sewage sludge and sediments from seven countries. BDE209 was analysed in four environmental matrices: sparrowhawk eggs (UK), glaucous gull eggs (Bear Island, Norway), sewage sludge (UK, Ireland and the Netherlands) and sediment (France, Germany, the Netherlands, UK and Ireland). BDE209 was detected in most of the glaucous gull and sparrow hawk eggs but neither increasing nor decreasing trends in these BDE209 levels were observed. An indication for debromination of BDE209 in sparrowhawk eggs was found. BDE209 concentrations in sediments ranged from very low ng/g (88 ng/g on an organic carbon (OC) basis) concentrations, in the rivers Elbe, Ems, Seine and the Outer Humber, to high µg/g (120 µg/g OC), in the Western Scheldt, Liverpool Bay and River Mersey. Apart from decreasing values in the Western Scheldt sediment no further decreases in BDE209 concentrations were observed over time, neither in sediment nor in sewage sludge showing that the voluntary emissions control program of the bromine industry only had a local effect. In contrast to the sewage sludge samples from the Netherlands (mean 355 ng/g dry weight (dw) or 1026 ng/g OC), the BDE209 concentrations in the UK increased at all sites from 2006 to 2011 (8092 ng/g dw or 22,367 ng/g OC). The BDE209 levels in several UK sediments and sewage sludge were still very high at the end of the program in 2012, most likely caused by frequent use of BDE209 in the textile industry. This may be indicative of the persistence of BDE209 and the limited degradation into lower brominated congeners in sediment, although it cannot be excluded that ongoing BDE209 emissions have played a role as well.

A schematic sampling protocol for contaminant monitoring in raptors.

Birds of prey, owls and falcons are widely used as sentinel species in raptor biomonitoring programmes. A major current challenge is to facilitate large-scale biomonitoring by coordinating contaminant monitoring activities and by building capacity across countries. This requires sharing, dissemination and adoption of best practices addressed by the Networking Programme Research and Monitoring for and with Raptors in Europe (EURAPMON) and now being advanced by the ongoing international COST Action European Raptor Biomonitoring Facility. The present perspective introduces a schematic sampling protocol for contaminant monitoring in raptors. We provide guidance on sample collection with a view to increasing sampling capacity across countries, ensuring appropriate quality of samples and facilitating harmonization of procedures to maximize the reliability, comparability and interoperability of data. The here presented protocol can be used by professionals and volunteers as a standard guide to ensure harmonised sampling methods for contaminant monitoring in raptors.

Contrasting long term temporal trends in perfluoroalkyl substances (PFAS) in eggs of the northern gannet (Morus bassanus) from two UK colonies.

We compared long-term (1977 to 2014) trends in concentrations of PFAS in eggs of the marine sentinel species, the Northern gannet (Morus bassanus), from the Irish Sea (Ailsa Craig) and the North Sea (Bass Rock). Concentrations of eight perfluorinated carboxylic acids (PFCAs) and three perfluorinated sulfonates (PFSAs) were determined and we report the first dataset on PFAS in UK seabirds before and after the PFOS ban. There were no significant differences in ∑PFAS or ∑PFSAs between both colonies. The ∑PFSAs dominated the PFAS profile (>80%); PFOS accounted for the majority of the PFSAs (98-99%). In contrast, ∑PFCAs concentrations were slightly but significantly higher in eggs from Ailsa Craig than in those from Bass Rock. The most abundant PFCAs were perfluorotridecanoate (PFTriDA) and perfluoroundecanoate (PFUnA) which, together with PFOA, comprised around 90% of the ∑PFCAs. The ∑PFSAs and ∑PFCAs had very different temporal trends. ∑PFSAs concentrations in eggs from both colonies increased significantly in the earlier part of the study but later declined significantly, demonstrating the effectiveness of the phasing out of PFOS production in the 2000s. In contrast, ∑PFCAs concentrations in eggs were constant and low in the 1970s and 1980s, suggesting minimal environmental contamination, but residues subsequently increased significantly in both colonies until the end of the study. This increase appeared driven by rises in long chain compounds, namely the odd chain numbered PFTriDA and PFUnA. PFOA, had a very different temporal trend from the other dominant acids, with an earlier rise in concentrations followed by a decline in the last 15 years in Ailsa Craig; later temporal trends in Bass Rock eggs were unclear. Although eggs from both colonies contained relatively low concentrations of PFAS, the majority had PFOS residues that exceeded a suggested Predicted No Effect Concentration and ~ 10% of the eggs exceeded a suggested Lowest-Observable-Adverse-Effect.

Concentration and origin of lead (Pb) in liver and bone of Eurasian buzzards (Buteo buteo) in the United Kingdom.

Ingestion of lead (Pb) derived from ammunition used in the hunting of game animals is recognised to be a significant potential source of Pb exposure of wild birds, including birds of prey. However, there are only limited data for birds of prey in Europe regarding tissue concentrations and origins of Pb. Eurasian buzzards (Buteo buteo) found dead in the United Kingdom during an 11-year period were collected and the concentrations of Pb in the liver and femur were measured. Concentrations in the liver consistent with acute exposure to Pb were found in 2.7% of birds and concentration in the femur consistent with exposure to lethal levels were found in 4.0% of individuals. Pb concentration in the femur showed no evidence of consistent variation among or within years, but was greater for old than for young birds. The Pb concentration in the liver showed no effect of the birds' age, but varied markedly among years and showed a consistent tendency to increase substantially within years throughout the UK hunting season for gamebirds. The resemblance of the stable isotope composition of Pb from buzzard livers to that of Pb from the types of shotgun ammunition most widely-used in the UK increased markedly with increasing Pb concentration in the liver. Stable isotope results were consistent with 57% of the mass of Pb in livers of all of the buzzards sampled being derived from shotgun pellets, with this proportion being 89% for the birds with concentrations indicating acute exposure to Pb. Hence, most of the Pb acquired by Eurasian buzzards which have liver concentrations likely to be associated with lethal and sublethal effects is probably obtained when they prey upon or scavenge gamebirds and mammals shot using Pb shotgun pellets.

Biological and anthropogenic predictors of metal concentration in the Eurasian otter, a sentinel of freshwater ecosystems.

Toxic metals have been linked to a range of adverse health effects in freshwater organisms. However, for higher vertebrates, there is little understanding of the large-scale drivers of exposure. We quantified toxic metal/semi-metal concentrations in a sentinel freshwater top predator, the Eurasian otter (Lutra lutra), across England and Wales, and determined how this varied with key natural and anthropogenic factors. We related liver concentrations in 278 otters that died between 2006 and 2017 to habitat biogeochemistry, proximity to point source contamination and to biological characteristics (length, sex, condition). Evidence for any positive association with putative anthropogenic sources (mining, human population, known discharges) was weak or lacking in nearly all cases, with the exception of a positive association between lead and human population density. Despite concerns that burgeoning use of nanosilver in consumer products might increase silver concentrations in waste waters, there was no increase over time. Spatial variation in soil/sediment pH, precipitation, and soil calcium oxide are indicated as significant predictors of metal concentrations in otters (higher cadmium and silver in areas with lower pH and higher rainfall, and higher chromium and lead in areas of lower calcium oxide). Liver chromium and nickel concentrations declined significantly over time (Cr 0.030 ± 1.2 to 0.015 ± 1.3 µg/g dry weight, Ni 0.0038 ± 1.2 to 0.00068 ± 1.5 µg/g, between 2006-2009 and 2014-2017), but other metals showed no temporal change. Biotic associations were important, with age related accumulation indicated for mercury and cadmium (as well as interactions with body condition). Our results suggest that larger-scale geochemical and hydrological processes are important in determining metal exposure in otters, and we provide an indication of risk factors that may be of relevance for freshwater vertebrates in other countries with well-developed water pollution management.

Lead contamination in raptors in Europe: A systematic review and meta-analysis.

Lead contamination is a widely recognised conservation problem for raptors worldwide. There are a number of studies in individual raptor species but those data have not been systematically evaluated to understand raptor-wide lead exposure and effects at a pan-European scale. To critically assess the extent of this problem, we performed a systematic review compiling all published data on lead in raptors (1983-2019) and, through a meta-analysis, determined if there was evidence for differences in exposure across feeding traits, geographical regions, between hunting and non-hunting periods, and changes over time. We also reviewed the impact of lead on raptors and the likely main source of exposure. We examined 114 studies that were unevenly distributed in terms of time of publication and the countries in which studies were performed. Peer-reviewed articles reported data for 39 raptor species but very few species were widely monitored across Europe. Obligate (vultures) and facultative scavengers (golden eagle, common buzzard and white-tailed sea eagle) accumulated the highest lead concentrations in tissues and generally were the species most at risk of lead poisoning. We found no evidence of a spatial or decadal trend in lead residues, but we demonstrated that high lead blood levels relate to hunting season. Exposure at levels associated with both subclinical and lethal effects is common and lead from rifle bullets and shot is often the likely source of exposure. Overall, our review illustrates the high incidence and ubiquity of lead contamination in raptors in Europe. However, we did not find studies that related exposure to quantitative impacts on European raptor populations nor detailed studies on the impact of mitigation measures. Such information is urgently needed and requires a more harmonised approach to quantifying lead contamination and effects in raptors across Europe.

High prevalence of the neonicotinoid clothianidin in liver and plasma samples collected from gamebirds during autumn sowing.

Since neonicotinoid insecticides were introduced to the agricultural market, evidence of the negative impacts of these systemic compounds on non-target species has accumulated. Birds are one of the largest groups of species to inhabit farmland, but the extent of neonicotinoid exposure in avian communities is poorly understood and very little is known about how any exposure may affect wild birds. Here, free-living gamebirds were used as a model group to measure the extent of avian exposure to the neonicotinoid clothianidin via seed treatment. During a typical sowing period of winter cereals treated with clothianidin, blood and liver samples were collected simultaneously from individual hunted gamebird carcasses, both pre- (n = 18) and post-sowing (n = 57) and were analysed for clothianidin via LC/MS-MS. Body weight, fat score and faecal parasite load were also quantified in the birds to ascertain whether any of these health parameters were associated with clothianidin exposure under field conditions. Clothianidin was detected in 6% of individuals sampled pre-sowing and 89% of individuals sampled post-sowing. The frequency of clothianidin detection in plasma samples and the concentration of clothianidin in liver and plasma samples decreased significantly between the first week and 2-4 weeks post-sowing. Faecal parasite load was positively associated with concentrations of clothianidin in the liver (but not plasma) of partridge species, but there was no association between clothianidin concentration and fat score or body weight, for either sample type. This study provides clear evidence that treated seed is a source of pesticide exposure for gamebirds following autumn sowing. These findings have implications for gamebirds worldwide where seed treatments are in use, and will aid the design of any future avian biomonitoring studies for agrochemical compounds.

Interactions between Environmental Contaminants and Gastrointestinal Parasites: Novel Insights from an Integrative Approach in a Marine Predator.

Environmental contaminants and parasites are ubiquitous stressors that can affect animal physiology and derive from similar dietary sources (co-exposure). To unravel their interactions in wildlife, it is thus essential to quantify their concurring drivers. Here, the relationship between blood contaminant residues (11 trace elements and 17 perfluoroalkyl substances) and nonlethally quantified gastrointestinal parasite loads was tested while accounting for intrinsic (sex, age, and mass) and extrinsic factors (trophic ecology inferred from stable isotope analyses and biologging) in European shags Phalacrocorax aristotelis. Shags had high mercury (range 0.65-3.21 µg g-1 wet weight, ww) and extremely high perfluorooctanoic acid (PFOA) and perfluorononanoic acid (PFNA) residues (3.46-53 and 4.48-44 ng g-1 ww, respectively). Males had higher concentrations of arsenic, mercury, PFOA, and PFNA than females, while the opposite was true for selenium, perfluorododecanoic acid (PFDoA), and perfluooctane sulfonic acid (PFOS). Individual parasite loads (Contracaecum rudolphii) were higher in males than in females. Females targeted pelagic-feeding prey, while males relied on both pelagic- and benthic-feeding organisms. Parasite loads were not related to trophic ecology in either sex, suggesting no substantial dietary co-exposure with contaminants. In females, parasite loads increased strongly with decreasing selenium:mercury molar ratios. Females may be more susceptible to the interactive effects of contaminants and parasites on physiology, with potential fitness consequences.