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

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

Feather corticosterone content in predatory birds in relation to body condition and hepatic metal concentration

This study investigated the feasibility of measuring corticosterone in feathers from cryo-archived raptor specimens, in order to provide a retrospective assessment of the activity of the stress axis in relation to contaminant burden. Feather samples were taken from sparrowhawk Accipiter nisus, kestrel Falco tinnunculus, buzzard Buteo buteo, barn owl Tyto alba, and tawny owl Strix aluco and the variation in feather CORT concentrations with respect to species, age, sex, feather position, and body condition was assessed. In sparrowhawks only, variation in feather CORT content was compared with hepatic metal concentrations. For individuals, CORT concentration (pg mm-1) in adjacent primary flight feathers (P5 and P6), and left and right wing primaries (P5), was statistically indistinguishable. The lowest concentrations of CORT were found in sparrowhawk feathers and CORT concentrations did not vary systematically with age or sex for any species. Significant relationships between feather CORT content and condition were observed in only tawny owl and kestrel. In sparrowhawks, feather CORT concentration was found to be positively related to the hepatic concentrations of five metals (Cd, Mn, Co, Cu, Mo) and the metalloid As. There was also a negative relationship between measures of condition and total hepatic metal concentration in males. The results suggest that some factors affecting CORT uptake by feathers remain to be resolved but feather CORT content from archived specimens has the potential to provide a simple effects biomarker for exposure to environmental contaminants

Levels of organochlorine pesticides are associated with amyloid aggregation in apex avian brains

Organochlorine (OC) pesticides pose a significant environmental risk to wildlife and humans and have been associated with Alzheimer’s disease (AD). This study aims to spectroscopically analyse brains from free-flying birds and link the results to OC exposure and consequent amyloid aggregation. As long-lived apex predators, predatory birds represent a sentinel species similar to humans. Therefore, the results have implications for both species and may also add to our understanding of the role OC pesticides play in the development of AD. Brains of wild sparrowhawks were analysed using ATR-FTIR and Raman spectroscopy and Congo red staining; results were correlated with OC pesticide concentrations in livers. Effects of OC exposure were sex and age dependant and associated alterations were seen in lipids and protein secondary structure. A shift from α-helix to β-sheet conformation of proteins indicated that concentrations of OC pesticides > 7.18 µg/g may lead to cerebral amyloid aggregation

How much do PCB toxic equivalents account for PHAH toxicity in predatory birds?

Various diffuse polyhalogenated aromatic hydrocarbons (PHAHs) exert common toxicity through the aryl hydrocarbon receptor (AhR). Apex predators spatially and temporally integrate diffuse contamination and simultaneous exposure can cause additive toxicity. We investigated the extent to which PCBs, still amongst the most prevalent PHAHs accumulated by predators, accounted for total PHAH toxicity in raptors and fish eating birds from Britain. We analysed egg or liver extracts from six species and compared chemically determined ΣPCB-TEQs concentrations with total AhR-mediated toxicity determined using the chemical-activated luciferase gene expression bioassay (CALUX-TEQ). Dioxin-like PCB profiles in eggs and livers were dominated by congeners 118, 105 and 167. ΣPCB-TEQ and CALUX-TEQ concentrations were positively associated but not in a 1:1 relationship. ΣPCB-TEQ were broadly similar to CALUX-TEQ concentrations in eggs and livers with CALUX-TEQ concentrations >50–80 and 160–320 pg g−1 lipid respectively, but were lower than CALUX-TEQ concentrations in less contaminated samples

Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife

Despite a long history of successful use, routine application of some anticoagulant rodenticides (ARs) may be at a crossroad due to new regulatory guidelines intended to mitigate risk. An adverse outcome pathway for ARs was developed to identify information gaps and end points to assess the effectiveness of regulations. This framework describes chemical properties of ARs, established macromolecular interactions by inhibition of vitamin K epoxide reductase, cellular responses including altered clotting factor processing and coagulopathy, organ level effects such as hemorrhage, organism responses with linkages to reduced fitness and mortality, and potential consequences to predator populations. Risk assessments have led to restrictions affecting use of some second-generation ARs (SGARs) in North America. While the European regulatory community highlighted significant or unacceptable risk of ARs to nontarget wildlife, use of SGARs in most EU member states remains authorized due to public health concerns and the absence of safe alternatives. For purposes of conservation and restoration of island habitats, SGARs remain a mainstay for eradication of invasive species. There are significant data gaps related to exposure pathways, comparative species sensitivity, consequences of sublethal effects, potential hazards of greater AR residues in genetically resistant prey, effects of low-level exposure to multiple rodenticides, and quantitative data on the magnitude of nontarget wildlife mortality

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

Diets of European polecat Mustela putorius in Great Britain during fifty years of population recovery

Following nineteenth-century declines, polecats Mustela putorius are recolonising Great Britain. Polecat diet relates to two potential risks to recovery. First, rabbits Oryctolagus cuniculus, which are important prey for polecats, have experienced extreme population fluctuations, with near extirpation due to myxomatosis in the 1950s, recovery in 1960s–1990s and declines in 1990s–2010s. Second, polecats are secondarily exposed to anticoagulant rodenticides by eating contaminated rodents, and the frequency of polecat exposure to rodenticides is increasing. We analysed stomach contents from 99 polecats collected in 2012–2016 and compared results with earlier studies. Lagomorphs were the most abundant prey (66% frequency of occurrence, 95% confidence interval 53–74%), followed by other mammals (12%, 4–18%), amphibians (10%, 3–16%) and birds (7%, 1–13%). Diet varied seasonally; lagomorph occurrence was highest in spring and summer and lowest in autumn. Dietary niche breadth was greater in the 1960s, when rabbits were scarce, than in other decades, but did not differ between the 1990s and 2010s, indicating that diets have not diversified with recent rabbit declines. This may be because rabbit abundance is not yet low enough to cause dietary diversification or because polecats were collected in areas where rabbits were still abundant. Rodents did not increase in diet between the 1990s and 2010s and still occur with < 10% frequency, indicating that rodents need not contribute much to diet to expose polecats to rodenticides. This potentially limits the effectiveness of management actions designed to minimise polecat exposure to contaminated rodent prey

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