Long-term trends of second generation anticoagulant rodenticides (SGARs) show widespread contamination of a bird-eating predator, the Eurasian Sparrowhawk (Accipiter nisus) in Britain.

Second generation anticoagulant rodenticides (SGARs) are widely used to control rodents around the world. However, contamination by SGARs is detectable in many non-target species, particularly carnivorous mammals or birds-of-prey that hunt or scavenge on poisoned rodents. The SGAR trophic transfer pathway via rodents and their predators/scavengers appears widespread, but little is known of other pathways of SGAR contamination in non-target wildlife. This is despite the detection of SGARs in predators that do not eat rodents, such as specialist bird-eating hawks. We used a Bayesian modelling framework to examine the extent and spatio-temporal trends of SGAR contamination in the livers of 259 Eurasian Sparrowhawks, a specialist bird-eating raptor, in regions of Britain during 1995-2015. SGARs, predominantly difenacoum, were detected in 81% of birds, with highest concentrations in males and adults. SGAR concentrations in birds were lowest in Scotland and higher or increasing in other regions of Britain, which had a greater arable or urban land cover where SGARs may be widely deployed for rodent control. However, there was no overall trend for Britain, and 97% of SGAR residues in Eurasian Sparrowhawks were below 100 ng/g (wet weight), which is a potential threshold for lethal effects. The results have potential implications for the population decline of Eurasian Sparrowhawks in Britain. Fundamentally, the results indicate an extensive and persistent contamination of the avian trophic transfer pathway on a national scale, where bird-eating raptors and, by extension, their prey appear to be widely exposed to SGARs. Consequently, these findings have implications for wildlife contamination worldwide, wherever these common rodenticides are deployed, as widespread exposure of non-target species can apparently occur via multiple trophic transfer pathways involving birds as well as rodents.

Continued Anticoagulant Rodenticide Exposure of Red-tailed Hawks (Buteo jamaicensis) in the Northeastern United States with an Evaluation of Serum for Biomonitoring.

Prior studies (2006-2016) in birds of prey admitted to a wildlife clinic in Massachusetts, USA, revealed widespread exposure to second-generation anticoagulant rodenticides (SGARs) among red-tailed hawks (Buteo jamaicensis, RTHAs). Continued monitoring of species for which historic data are available can reveal trends in exposure that aid in evaluating the effectiveness of risk-mitigation measures. While the majority of exposure-monitoring studies utilize liver tissue collected postmortem, antemortem modalities, such as serum analysis, may be desirable for risk assessments in certain populations. However, the sensitivity of serum for detecting anticoagulant rodenticides (ARs) is not well studied. Paired liver and serum samples from 43 RTHAs were evaluated from 2017 to 2019. In liver tissue, 100% of birds were positive for ARs, with the SGARs brodifacoum, bromadiolone, and difethialone identified most frequently; 91% of birds had liver residues of 2 to 4 ARs. These findings represent the highest exposure both to ARs overall and to multiple ARs in RTHAs compared to previous studies. All birds diagnosed with AR toxicosis (n = 14) were positive for ARs in serum; however, all subclinically exposed birds (n = 29) were negative in serum. These data show that exposure to SGARs remains widespread in RTHAs in this geographic area. In addition, although serum analysis is not sensitive for detecting sublethal exposures in RTHAs, it can potentially support a diagnosis of AR toxicosis in conjunction with other consistent signs. Environ Toxicol Chem 2020;39:2325-2335. © 2020 SETAC.

Pheomelanin synthesis varies with protein food abundance in developing goshawks.

The accumulation of the amino acid cysteine in lysosomes produces toxic substances, which are avoided by a gene (CTNS) coding for a transporter that pumps cystine out of lysosomes. Melanosomes are lysosome-related organelles that synthesize melanins, the most widespread pigments in animals. The synthesis of the orange melanin, termed pheomelanin, depends on cysteine levels because the sulfhydryl group is used to form the pigment. Pheomelanin synthesis may, therefore, be affected by cysteine homeostasis, although this has never been explored in a natural system. As diet is an important source of cysteine, here we indirectly tested for such an effect by searching for an association between food abundance and pheomelanin content of feathers in a wild population of Northern goshawk Accipiter gentilis. As predicted on the basis that CTNS expression may inhibit pheomelanin synthesis and increase with food abundance as previously found in other strictly carnivorous birds, we found that the feather pheomelanin content in nestling goshawks, but not in adults, decreased as the abundance of prey available to them increased. In contrast, variation in the feather content of the non-sulphurated melanin form (eumelanin) was only explained by sex in both nestlings and adults. We also found that the feather pheomelanin content of nestlings was negatively related to that of their mothers, suggesting a relevant environmental influence on pheomelanin synthesis. Overall, our findings suggest that variation in pheomelanin synthesis may be a side effect of the maintenance of cysteine homeostasis. This may help explaining variability in the expression of pigmented phenotypes.

Pharmacokinetics of a concentrated buprenorphine formulation in red-tailed hawks (Buteo jamaicensis).

OBJECTIVE To determine the pharmacokinetics and sedative effects of 2 doses of a concentrated buprenorphine formulation after SC administration to red-tailed hawks (Buteo jamaicensis). ANIMALS 6 adult red-tailed hawks. PROCEDURES Concentrated buprenorphine (0.3 mg/kg, SC) was administered to all birds. Blood samples were collected at 10 time points over 24 hours after drug administration to determine plasma buprenorphine concentrations. After a 4-week washout period, the same birds received the same formulation at a higher dose (1.8 mg/kg, SC), and blood samples were collected at 13 time points over 96 hours. Hawks were monitored for adverse effects and assigned agitation-sedation scores at each sample collection time. Plasma buprenorphine concentrations were quantified by liquid chromatography-tandem mass spectrometry. RESULTS Mean time to maximum plasma buprenorphine concentration was 7.2 minutes and 26.1 minutes after administration of the 0.3-mg/kg and 1.8-mg/kg doses, respectively. Plasma buprenorphine concentrations were > 1 ng/mL for mean durations of 24 and 48 hours after low- and high-dose administration, respectively. Mean elimination half-life was 6.23 hours for the low dose and 7.84 hours for the high dose. Mean agitation-sedation scores were higher (indicating some degree of sedation) than the baseline values for 24 hours at both doses. No clinically important adverse effects were observed. CONCLUSIONS AND CLINICAL RELEVANCE Concentrated buprenorphine was rapidly absorbed, and plasma drug concentrations considered to have analgesic effects in other raptor species were maintained for extended periods. Most birds had mild to moderate sedation. Additional studies are needed to evaluate the pharmacodynamics of these doses of concentrated buprenorphine in red-tailed hawks.

Per- and polyfluoroalkyl substances in plasma and feathers of nestling birds of prey from northern Norway.

Plasma samples from nestlings of two top predators, White-tailed eagle (Haliaeetus albicilla) and Northern goshawk (Accipiter gentilis) from northern Norway were analysed for a wide range of per- and polyfluoroalkyl substances (PFASs). Body feathers from the White-tailed eagles were also analysed and significant associations between specific PFASs in blood plasma and body feathers were found (0.36

Pharmacokinetics of a single dose of voriconazole administered orally with and without food to red-tailed hawks (Buteo jamaicensus).

OBJECTIVE To determine the pharmacokinetics of voriconazole administered PO with or without food to red-tailed hawks (Buteo jamaicensus) and whether any observed variability could be explained by measured covariates to inform dose adjustments. ANIMALS 7 adult red-tailed hawks. PROCEDURES In a crossover study design, hawks were randomly assigned to first receive voriconazole (15 mg/kg, PO) injected into a dead mouse (n = 3; fed birds) or without food (4; unfed birds). Sixteen days later, treatments were reversed. Blood samples were collected at various points to measure plasma voriconazole concentrations by ultraperformance liquid chromatography. Pharmacokinetic data were analyzed by noncompartmental methods and fit to a compartmental model through nonlinear mixed-effects regression, with feeding status and body weight investigated as covariates. RESULTS Voriconazole was well absorbed, with quantifiable plasma concentrations up to 24 hours after administration. Mean plasma half-life was approximately 2 hours in fed and unfed birds. Administration of the voriconazole in food delayed absorption, resulting in a significant delay in time to maximum plasma concentration. The final compartmental model included a categorical covariate to account for this lag in absorption as well as body weight as a covariate of total body clearance (relative to unknown bioavailability). CONCLUSIONS AND CLINICAL RELEVANCE A single dose of voriconazole (15 mg/kg) administered PO to red-tailed hawks resulted in mean plasma voriconazole concentrations greater than the targeted value (1 µg/mL). Additional studies with larger sample sizes and multidose regimens are required before the model developed here can be applied in clinical settings.

Temporal trends in mercury concentrations in raptor flight feathers stored in an environmental specimen bank in Galicia (NW Spain) between 2000 and 2013.

Temporal trends in Hg concentrations were investigated in primary flight feathers from 319 specimens of three birds of prey: P7 in the northern goshawk (Accipiter gentilis), P6 in the common buzzard (Buteo buteo) and P5 in the tawny owl (Strix aluco). The samples were stored in a regional environmental specimen bank and belonged to specimens which died between 2000 and 2013 in Galicia (NW Spain). We would expect to see a decline in Hg concentrations across the study period, as data of atmospheric emissions show a gradual reduction of this pollutant in Europe in the last two decades. The study did not reveal any temporal pattern in Hg concentrations of feathers in any of the three species for the study period, may be due to the persistence of Hg in the environment, but showed a low level of contamination by this metal in the study area. In addition, the results show high intra-specific, as well as, inter-annual and inter-specific variability in data, mainly attributed to the level of exposure of the raptors to this pollutant and to the biomagnification process of Hg through food chains. These findings indicate that the high variability can be a limiting factor in the use of raptors for biomonitoring temporal patterns of Hg, but nevertheless, the technique provides qualitative information about the amount of Hg that reach the top of the terrestrial food chains.

Ground Squirrel Shooting and Potential Lead Exposure in Breeding Avian Scavengers.

Recreational ground squirrel shooting is a popular activity throughout the western United States and serves as a tool for managing ground squirrel populations in agricultural regions. Belding's ground squirrels (Spermophilus beldingi) are routinely shot in California, Nevada, and Oregon across habitats that overlap with breeding avian scavengers. Ground squirrels shot with lead (Pb)-based bullets may pose a risk to avian scavengers if they consume carcasses containing Pb fragments. To assess the potential risk to breeding avian scavengers we developed a model to estimate the number, mass, and distribution of Pb fragments in shot ground squirrels using radiographic images. Eighty percent of shot carcasses contained detectible Pb fragments with an average of 38.6 mg of Pb fragments. Seven percent of all carcasses contained Pb fragment masses exceeding a lethal dose for a model raptor nestling (e.g. American kestrel Falco sparverius). Bullet type did not influence the number of fragments in shot ground squirrels, but did influence the mass of fragments retained. Belding's ground squirrels shot with .17 Super Mag and unknown ammunition types contained over 28 and 17 times more mass of Pb fragments than those shot with .22 solid and .22 hollow point bullets, respectively. Ground squirrel body mass was positively correlated with both the number and mass of Pb fragments in carcasses, increasing on average by 76% and 56% respectively across the range of carcass masses. Although the mass of Pb retained in ground squirrel carcasses was small relative to the original bullet mass, avian scavenger nestlings that frequently consume shot ground squirrels may be at risk for Pb-induced effects (e.g., physiology, growth, or survival). Using modeling efforts we found that if nestling golden eagles (Aquila chrysaetos), red-tailed hawks (Buteo jamaicensis), and Swainson's hawks (B. swainsoni) consumed shot ground squirrels proportionately to the nestling's mass, energy needs, and diet, 100% of the nestling period would exceed a 50% reduction in delta-aminolevulinic acid dehydratase production threshold, the last 13-27% of the nestling stage would exceed a reduced growth rate threshold, but no nestlings would be expected to exceed a level of Pb ingestion that would be lethal.

Unintentional wildlife poisoning and proposals for sustainable management of rodents.

In Europe, bromadiolone, an anticoagulant rodenticide authorized for plant protection, may be applied intensively in fields to control rodents. The high level of poisoning of wildlife that follows such treatments over large areas has been frequently reported. In France, bromadiolone has been used to control water voles (Arvicola terrestris) since the 1980s. Both regulation and practices of rodent control have evolved during the last 15 years to restrict the quantity of poisoned bait used by farmers. This has led to a drastic reduction of the number of cases of poisoned wildlife reported by the French surveillance network SAGIR. During the autumn and winter 2011, favorable weather conditions and high vole densities led to the staging of several hundreds of Red Kites (Milvus milvus) in the Puy-de-Dôme department (central France). At the same time, intensive treatments with bromadiolone were performed in this area. Although no misuse has been mentioned by the authorities following controls, 28 Red Kites and 16 Common Buzzards (Buteo buteo) were found dead during surveys in November and December 2011. For all these birds, poisoning by bromadiolone as the main cause of death was either confirmed or highly suspected. Other observations suggest a possible impact of bromadiolone on the breeding population of Red Kites in this area during the spring 2011. French regulation of vole control for plant protection is currently under revision, and we believe this event calls for more sustainable management of rodent outbreaks. Based on large-scale experiments undertaken in eastern France, we propose that direct control of voles at low density (with trapping or limited chemical treatments) and mechanical destruction of vole tunnels, mole control, landscape management, and predator fostering be included in future regulation because such practices could help resolve conservation and agricultural issues.

Anticoagulant rodenticides in red-tailed hawks, Buteo jamaicensis, and great horned owls, Bubo virginianus, from New Jersey, USA, 2008-2010.

Liver samples from red-tailed hawks (Buteo jamaicensis) and great horned owls (Bubo virginianus) were analyzed for anticoagulant rodenticides. Residues of one or more second generation anticoagulant rodenticides (SGARs) were detected in 81 % of red-tailed hawks and 82 % of great horned owls. The most frequently detected SGAR was brodifacoum, which was detected in 76 % of red-tailed hawks and 73 % of great horned owls. Bromadiolone was detected in 20 % of red-tailed hawks and 27 % of great horned owls. Difenacoum was detected in one great horned owl. No other ARs were detected. There were no significant differences between species in the frequency of detection or concentration of brodifacoum or bromadiolone. There was a marginally significant difference (p = 0.0497) between total SGAR residues in red-tailed hawks (0.117 mg/kg) and great horned owls (0.070 mg/kg). There were no seasonal differences in the frequency of detection or concentration of brodifacoum in red-tailed hawks. The data suggest that SGARs pose a significant risk of poisoning to predatory birds in New Jersey.

Liver lead concentrations in raptors in New Jersey, USA, 2008-2010.

Lead exposure in New Jersey raptors was assessed by analyzing liver samples from carcasses obtained from wildlife rehabilitators. Samples were collected from 221 individuals representing 13 species. Concentrations were within the range of normal background exposure in 12 species. One red-tailed hawk had a liver lead concentration consistent with clinical poisoning (7.4 µg/g wet weight), which represents an incidence of 1% (1/104) in that species and 0.5% (1/221) in the overall sample. A second red-tailed hawk had a liver lead concentration consistent with subclinical exposure (2.1 µg/g wet weight). The combined incidence of elevated exposure (subclinical exposure + clinical poisoning) was 2% (2/104) in red-tailed hawks and 1% (2/221) in the overall sample.

Second generation anticoagulant rodenticides in predatory birds: Probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada.

Second-generation anticoagulant rodenticides (SGARs) are widely used to control rodent pests but exposure and poisonings occur in non-target species, such as birds of prey. Liver residues are often analysed to detect exposure in birds found dead but their use to assess toxicity of SGARs is problematic. We analysed published data on hepatic rodenticide residues and associated symptoms of anticoagulant poisoning from 270 birds of prey using logistic regression to estimate the probability of toxicosis associated with different liver SGAR residues. We also evaluated exposure to SGARs on a national level in Canada by analysing 196 livers from great horned owls (Bubo virginianus) and red-tailed hawks (Buteo jamaicensis) found dead at locations across the country. Analysis of a broader sample of raptor species from Quebec also helped define the taxonomic breadth of contamination. Calculated probability curves suggest significant species differences in sensitivity to SGARs and significant likelihood of toxicosis below previously suggested concentrations of concern (<0.1mg/kg). Analysis of birds from Quebec showed that a broad range of raptor species are exposed to SGARs, indicating that generalised terrestrial food chains could be contaminated in the vicinity of the sampled areas. Of the two species for which we had samples from across Canada, great horned owls are exposed to SGARs to a greater extent than red-tailed hawks and the liver residue levels were also higher. Using our probability estimates of effect, we estimate that a minimum of 11% of the sampled great horned owl population is at risk of being directly killed by SGARs. This is the first time the potential mortality impact of SGARs on a raptor population has been estimated.

Pharmacokinetics of butorphanol tartrate in red-tailed hawks (Buteo jamaicensis) and great horned owls (Bubo virginianus).

OBJECTIVE: To determine the pharmacokinetics of butorphanol tartrate after IV and IM single-dose administration in red-tailed hawks (RTHs) and great horned owls (GHOs). ANIMALS: 6 adult RTHs and 6 adult GHOs. PROCEDURES: Each bird received an injection of butorphanol (0.5 mg/kg) into either the right jugular vein (IVj) or the pectoral muscles in a crossover study (1-week interval between treatments). The GHOs also later received butorphanol (0.5 mg/kg) via injection into a medial metatarsal vein (IVm). During each 24-hour postinjection period, blood samples were collected from each bird; plasma butorphanol concentrations were determined via liquid chromatography-mass spectrometry. RESULTS: 2- and 1-compartment models best fit the IV and IM pharmacokinetic data, respectively, in both species. Terminal half-lives of butorphanol were 0.94 +/- 0.30 hours (IVj) and 0.94 +/- 0.26 hours (IM) for RTHs and 1.79 +/- 1.36 hours (IVj), 1.84 +/- 1.56 hours (IM), and 1.19 +/- 0.34 hours (IVm) for GHOs. In GHOs, area under the curve (0 to infinity) for butorphanol after IVj or IM administration exceeded values in RTHs; GHO values after IM and IVm administration were less than those after IVj administration. Plasma butorphanol clearance was significantly more rapid in the RTHs. Bioavailability of butorphanol administered IM was 97.6 +/- 33.2% (RTHs) and 88.8 +/- 4.8% (GHOs). CONCLUSIONS AND CLINICAL RELEVANCE: In RTHs and GHOs, butorphanol was rapidly absorbed and distributed via all routes of administration; the drug's rapid terminal half-life indicated that published dosing intervals for birds may be inadequate in RTHs and GHOs.

Nutritional condition and serum biochemistry for free-living Swainson's Hawks wintering in central Argentina.

We assessed the nutritional condition and established reference values for serum chemistry parameters in a long distance migrant bird of prey, the Swainson's Hawk (Buteo swainsoni), wintering in central Argentina. We analyzed serum concentration of urea, uric acid, cholesterol, and triglycerides and assessed age and sex related differences in these parameters. A body condition index was obtained from the resultant residuals of the regression of body mass and a morphometric measure. No statistical differences were observed among sex and age groups for urea, uric acid and triglyceride serum concentration. However, cholesterol concentration differed among male and female hawks, which could be related to the gain of body mass in wintering grounds at differential rates. The mean values of the four parameters were in the range of those recorded in the Common Buzzard (Buteo buteo), indicating good nutritional condition of the population we studied. Forearm length was the morphometric variable that better correlated with body mass. The resultant body condition index was only correlated with triglyceride concentration, suggesting that this index could be valuable in future work dealing with the assessment of body fat storage in wintering and breeding hawks, as well as in stopover points on the migratory route.