Anticoagulant Rodenticide Toxicity in Terrestrial Raptors: Tools to Estimate the Impact on Populations in North America and Globally.

Anticoagulant rodenticides (ARs) have caused widespread contamination and poisoning of predators and scavengers. The diagnosis of toxicity proceeds from evidence of hemorrhage, and subsequent detection of residues in liver. Many factors confound the assessment of AR poisoning, particularly exposure dose, timing and frequency of exposure, and individual and taxon-specific variables. There is a need, therefore, for better AR toxicity criteria. To respond, we compiled a database of second-generation anticoagulant rodenticide (SGAR) residues in liver and postmortem evaluations of 951 terrestrial raptor carcasses from Canada and the United States, 1989 to 2021. We developed mixed-effects logistic regression models to produce specific probability curves of the toxicity of ∑SGARs at the taxonomic level of the family, and separately for three SGARs registered in North America, brodifacoum, bromadiolone, and difethialone. The ∑SGAR threshold concentrations for diagnosis of coagulopathy at 0.20 probability of risk were highest for strigid owls (15 ng g-1) lower and relatively similar for accipitrid hawks and eagles (8.2 ng g-1) and falcons (7.9 ng g-1), and much lower for tytonid barn owls (0.32 ng g-1). These values are lower than those we found previously, due to compilation and use of a larger database with a mix of species and source locations, and also to refinements in the statistical methods. Our presentation of results on the family taxonomic level should aid in the global applicability of the numbers. We also collated a subset of 440 single-compound exposure events and determined the probability of SGAR-poisoning symptoms as a function of SGAR concentration, which we then used to estimate relative SGAR toxicity and toxic equivalence factors: difethialone, 1, brodifacoum, 0.8, and bromadiolone, 0.5. Environ Toxicol Chem 2024;43:988-998. © 2024 His Majesty the King in Right of Canada and The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC Reproduced with the permission of the Minister of Environment and Climate Change Canada.

Contaminant biomonitoring augmented with a qPCR array indicates hepatic mRNA gene expression effects in wild-collected seabird embryos.

Birds can bioaccumulate persistent contaminants, and maternal transfer to eggs may expose embryos to concentrations sufficient to cause adverse effects during sensitive early-life stages. However, using tissue residue concentrations alone to infer whether contaminant effects are occurring suffers from uncertainty, and efficient, sensitive biomarkers remain limited in wildlife. We studied relationships between whole embryo contaminant concentrations (total mercury, organochlorine pesticides, perfluoroalkyl substances, polychlorinated biphenyls, and halogenated flame retardants) together with mRNA expression in embryonic liver tissue from a Pacific Ocean seabird, the rhinoceros auklet (Cerorhinca monocerata). Fresh eggs were collected, incubated under controlled conditions, and from the pre-hatch embryo, hepatic RNA was extracted for qPCR array analysis to measure gene expression (2-∆Cq), while the remaining embryo was analyzed for contaminant residues. Contaminant and gene expression data were assessed with a combination of multivariate approaches and linear models. Results indicated correlations between embryonic total mercury and several genes such as sepp1, which encodes selenoprotein P. Correlation between the biotransformation gene cyp1a4 and the C7 perfluoroalkyl carboxylic acid PFHpA was also evident. This study demonstrates that egg collection from free-living populations for contaminant biomonitoring programs can relate chemical residues to in ovo mRNA gene expression effects in embryo hepatic tissue.

Perfluoroalkyl Substances in Seabird Eggs from Canada's Pacific Coast: Temporal Trends (1973-2019) and Interspecific Patterns.

Whether perfluoroalkyl sulfonates (PFSAs) and perfluoroalkyl carboxylates (PFCAs) are responding to legislative restrictions and showing decreasing trends in top marine predators that range across the eastern North Pacific Ocean is unclear. Here, we examined longer-term temporal trends (1973-2019) of 4 PFSAs and 13 PFCAs, as well stable isotopes of δ13C and δ15N, in the eggs of 4 seabird species sampled along a nearshore-offshore gradient; double-crested cormorants (Nannopterum auritum), pelagic cormorants (Urile pelagicus), rhinoceros auklets (Cerorhinca monocerata), and Leach's storm-petrels (Hydrobates leucorhous) from the Pacific coast of British Columbia, Canada. PFOS was the most abundant PFSA (79-94%) detected in all eggs regardless of colony and year, with the highest concentrations, on average, measured in auklet eggs (mean = 58 ng g-1, range = 11-286 ng g-1 ww). Perfluoroundecanoic acid (PFUdA) and perfluorotridecanoic acid (PFTriDA) were the dominant long-chain PFCAs (≥30% combined). The majority of PFSAs (including PFOS) are statistically declining (p < 0.001) in the eggs of all 4 species with PFOS half-lives ranging from 2.6 to 7.8 years. Concentrations of long-chain PFCAs exhibited a trajectory comprised of linear increases and second-order declines, suggesting that the rate of uptake of PFCAs is slowing or leveling off. These trends are consistent with the voluntarily ceased production of PFSAs by 3M circa 2000-2003 and are among the first from the northeast Pacific to indicate a positive response to several regulations and restrictions on PFCAs from facility emissions and product content.

Assessing plastic ingestion in birds of prey from British Columbia, Canada.

Since first being introduced for public use in the 1960s, plastic has become one of the most pervasive and ubiquitous forms of pollution globally. The potential fate and effects of plastic pollution on birds is a rapidly growing area of research, but knowledge of terrestrial and freshwater species is limited. Birds of prey have been particularly understudied, with no published data on plastic ingestion in raptors in Canada to date, and very few studies globally. To assess the ingestion of plastic in raptors, we analysed the contents of the upper gastrointestinal tracts from a total of 234 individuals across 15 raptor species, collected between 2013 and 2021. Upper gastrointestinal tracts were assessed for plastics and anthropogenic particles > 2 mm in size. Of the 234 specimens examined, only five individuals across two species had evidence of retained anthropogenic particles in the upper gastrointestinal tract. Two of 33 bald eagles (Haliaeetus leucocephalus, 6.1%) had retained plastics in the gizzard, while three of 108 barred owls (Strix varia, 2.8%) had retained plastic and non-plastic anthropogenic litter. The remaining 13 species were negative for particles > 2 mm in size (N = 1-25). These results suggest that most hunting raptor species do not appear to ingest and retain larger anthropogenic particles, though foraging guild and habitat may influence risk. We recommend that future research investigate microplastic accumulation in raptors, in order to gain a more holistic understanding of plastic ingestion in these species. Future work should also focus on increasing sample sizes across all species to improve the ability to assess landscape- and species-level factors that influence vulnerability and susceptibility of plastic pollution ingestion.

Temporal trends (1968-2019) of legacy persistent organic pollutants (POPs) in seabird eggs from the northeast Pacific: Is it finally twilight for old POPs?

Legacy persistent organic pollutants (POPs), such as organochlorine pesticides (OCs) and polychlorinated biphenyls (PCBs), are known to persist in the marine environment; however, whether concentrations of these POPs have decreased or stabilized from Canada's Pacific coast in recent years is unclear. Here, we examined temporal trends of various legacy POPs in the eggs of five seabird species; two cormorants (Nannopterum auritum and Urile pelagicus), an auklet (Cerorhinca monocerata), a murrelet (Synthliboramphus antiquus), and a storm-petrel (Hydrobates leucorhous), sampled 1968 to 2019 from 23 colonies along the Pacific coast of British Columbia, Canada. The contaminant profile in the eggs of all species and sampling years was dominated by ΣPCBs, followed by ΣDDT (mostly p,p'-DDE), ΣHCH (ß-HCH), ΣCHLOR (oxychlordane), and ΣCBz (HCB). ΣOC and ΣPCB concentrations were generally higher in double-crested cormorant eggs than in the other four species. The majority of legacy POPs are either significantly declining (e.g. p,p'-DDE, HCB, HE, oxychlordane, ΣPCBs) or showing no directional change over time (ΣMirex) in the eggs of our monitoring species. Contaminants such as α-HCH, cis- and trans-chlordane, p,p'-DDT, dieldrin, and octachlorostyrene also showed evidence of downward trends, largely influenced by non-detect values during more recent sampling periods. Increasing trends were observed for ß-HCH in the eggs of some species; however, mean concentrations eventually returned to early 2000 levels by the end of the study period. Although bulk δ15N and δ13C egg values varied interannually, compound-specific amino acid analyses suggested no major changes in trophic position or baseline food web signature. Temporal trends observed here were comparable to those found in other seabird species and pelagic food webs. As most legacy POPs in our data set were at very low levels in recent years, we support the general consensus that it is indeed the twilight years for old POPs, and we attribute these declines largely to voluntary regulations and international restrictions on the production and use of these compounds, and thus their release into the marine environment.

Anticoagulant Rodenticide Contamination of Terrestrial Birds of Prey from Western Canada: Patterns and Trends, 1988-2018.

As the dominant means for control of pest rodent populations globally, anticoagulant rodenticides (ARs), particularly the second-generation compounds (SGARs), have widely contaminated nontarget organisms. We present data on hepatic residues of ARs in 741 raptorial birds found dead or brought into rehabilitation centers in British Columbia, Canada, over a 30-year period from 1988 to 2018. Exposure varied by species, by proximity to residential areas, and over time, with at least one SGAR residue detected in 74% of individuals and multiple residues in 50% of individuals. By comparison, we detected first-generation compounds in <5% of the raptors. Highest rates of exposure were in barred owls (Strix varia), 96%, and great horned owls (Bubo virginianus), 81%, species with diverse diets, including rats (Rattus norvegicus and Rattus rattus), and inhabiting suburban and intensive agricultural habitats. Barn owls (Tyto alba), mainly a vole (Microtus) eater, had a lower incidence of exposure of 65%. Putatively, bird-eating raptors also had a relatively high incidence of exposure, with 75% of Cooper's hawks (Accipiter cooperii) and 60% of sharp-shinned hawks (Accipiter striatus) exposed. Concentrations of SGARs varied greatly, for example, in barred owls, the geometric mean ∑SGAR = 0.13, ranging from <0.005 to 1.81 µg/g wet weight (n = 208). Barred owls had significantly higher ∑SGAR concentrations than all other species, driven by significantly higher bromadiolone concentrations, which was predicted by the proportion of residential land within their home ranges. Preliminary indications that risk mitigation measures implemented in 2013 are having an influence on exposure include a decrease in mean concentrations of brodifacoum and difethialone in barred and great horned owls and an increase in bromodialone around that inflection point. Environ Toxicol Chem 2022;41:1903-1917. © 2022 Her Majesty the Queen in Right of Canada. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC. Reproduced with the permission of the Minister of Environment and Climate Change Canada.

Exposure to persistent organic pollutants is linked to over-wintering latitude in a Pacific seabird, the rhinoceros auklet, Cerorhinca monocerata.

Seabirds are wide-ranging organisms often used to track marine pollution, yet the effect of migration on exposure over the annual cycle is often unclear. We used solar geolocation loggers and stable isotope analysis to study the effects of post breeding dispersal and diet on persistent organic pollutant (POP) and mercury (Hg) burdens in rhinoceros auklets, Cerorhinca monocerata, breeding on islands along the Pacific Coast of Canada. Hg and four classes of POPs were measured in auklet eggs: organochlorine insecticides (OCs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and perfluoralkyl substances (PFASs). Stable isotope values of adult breast feathers grown during winter were used in conjunction with geolocation to elucidate adult wintering latitude. Wintering latitude was the most consistent and significant predictor of some POP and of Hg concentrations in eggs. The magnitude and pattern of exposure varied by contaminant, with ∑PCBs, ∑PBDEs and DDE decreasing with wintering latitude, and mirex, perfluoro-n-tridecanoic acid, and Hg increasing with latitude. We suggest that concentrations of these contaminants in rhinoceros auklet eggs are influenced by variation in uptake at adult wintering locations related to anthropogenic inputs and oceanic and atmospheric transport.

Influence of overwinter distribution on exposure to persistent organic pollutants (POPs) in seabirds, ancient murrelets (Synthliboramphus antiquus), breeding on the Pacific coast of Canada.

Assessing the fate of both legacy and newer persistent organic pollutants (POPs) is an ongoing challenge. Top predators, including seabirds, are effective monitors of POPs because they forage over a range of marine habitats, integrating signals over space and time. However, migration patterns can make unravelling contaminant sources, and potentially assessments of the effectiveness of regulations, challenging if chemicals are acquired at distant sites. In 2014, we fitted geolocators on ancient murrelets (Synthliboramphus antiqueus) at four colonies on the Pacific Coast of Canada to obtain movement data throughout an annual cycle. All birds underwent a post-breeding moult in the Bering Sea. Around one-third then returned to overwinter on the British Columbia (BC) coast while the rest migrated to overwinter in waters along the north Asian coast. Such a stark difference in migration destination provided an opportunity to examine the influence of wintering location on contaminant signals. In summer 2015, we collected blood samples from returned geo-tagged birds and analyzed them for a suite of contaminants, including polybrominated diphenyl ethers (PBDEs), non-PBDE halogenated flame retardants, perfluoroalkyl substances (PFASs), organochlorines, and mercury. Feathers were also collected and analyzed for stable isotopes (δ13C, δ15N, and δ34S). We found no significant differences in blood concentrations of any contaminant between murrelets from the two different overwinter areas, a result that indicates relatively rapid clearance of POPs accumulated during winter. Spatial variation in diet (i.e., δ13C) was associated with both BDE-47 and -99 concentrations. However, individual variation in trophic level had little influence on concentrations of any other examined contaminants. Thus, blood from these murrelets is a good indicator of recent, local contaminants, as most signals appear independent of overwintering location.

Effects of halogenated contaminants on reproductive development in wild mink (Neovison vison) from locations in Canada.

The concept of the Anthropocene, that humans are now re-engineering global ecosystems, is in part evidenced by the pervasive pollution by persistent organic pollutants (POPs). Certain POPs are hormone mimics and can disrupt endocrine and hence reproductive processes, shown mainly by laboratory studies with model species. There are, in contrast, fewer confirmations of such disruption from eco-epidemiological studies of wild mammals. Here we used the American mink (Neovison vison) as a sentinel species for such a study. Over the period 1998-2006, 161 mink carcasses were obtained from commercial trappers in the Canadian provinces of British Columbia and Ontario. Mink were aged, sexed, measured, and body condition assessed. Livers were analyzed either individually or pooled for organochlorine (OC) pesticides, polychlorinated biphenyls (PCBs), and subsets for polybrominated diphenyl ethers (PBDEs). We primarily addressed whether contaminants affected male reproductive development by measuring baculum size and assessing the influences of age and body condition. We also considered the influence of spatial variation on relative exposure and size of baculum. Statistical models separated by age class revealed that significant relationships between baculum length or mass and juvenile mink were mostly positive, whereas for adults and first year mink they were mostly negative. A significant negative relationship for adult mink was determined between DDE and both baculum length and mass. For juvenile mink we found significant positive relationships between ∑PCBs, DDE and ∑PBDEs with baculum length. Our results provide some indication of negative effects of halogenated contaminants on male reproductive development in wild mink, and the most likely candidate chemical is the confirmed anti-androgenic compound, DDE, rather than PCBs or other compounds.

Increased rodenticide exposure rate and risk of toxicosis in barn owls (Tyto alba) from southwestern Canada and linkage with demographic but not genetic factors.

Among many anthropogenic drivers of population decline, continual rapid urbanization and industrialization pose major challenges for the survival of wildlife species. Barn owls (Tyto alba) in southwestern British Columbia (BC) face a multitude of threats ranging from habitat fragmentation to vehicle strikes. They are also at risk from secondary poisoning of second-generation anticoagulant rodenticides (SGARs), a suite of toxic compounds which at high doses results in a depletion of blood clotting factors leading to internal bleeding and death. Here, using long-term data (N = 119) for the hepatic residue levels of SGAR, we assessed the risk of toxicosis from SGAR for the BC barn owl population over the past two decades. We also investigated whether sensitivity to SGAR is associated with genetic factors, namely Single Nucleotide Polymorphisms (SNPs) found in the CYP2C45 gene of barn owls. We found that residue concentration for total SGAR was significantly higher in 2006-2013 (141 ng/g) relative to 1992-2003 (57 ng/g). The proportion of owls exposed to multiple SGAR types was also significantly higher in 2006-2013. Those measures accordingly translate directly into an increase in toxicosis risk level. We also detected demographic differences, where adult females showed on average lower concentration of total SGAR (64 ng/g) when compared to adult males (106 ng/g). Juveniles were overall more likely to show signs of toxicosis than adults (33.3 and 6.9 %, respectively), and those symptoms were positively predicted by SGAR concentrations. We found no evidence that SNPs in the CYP2C45 gene of barn owls were associated with intraspecific variation in SGAR sensitivity. We recommend several preventative measures be taken to minimize wildlife exposure to SGAR.

Mercury in Forage Fish from Mexico and Central America: Implications for Fish-Eating Birds.

Mercury (Hg) is a global contaminant of aquatic food chains. Aquatic birds, such as the osprey (Pandion haliaetus), with migratory populations breeding in Canada and the northern United States and wintering in the Central and South America, can be exposed to mercury on both the breeding and wintering ranges. We examined Hg levels in 14 fish taxa from 24 osprey wintering sites identified from satellite telemetry. Our main goal was to determine whether fish species that feature in the diet of overwintering and resident fish-eating birds reached toxicity thresholds for Hg. Mean Hg levels in fish whole carcasses ranged from a high of 0.18 µg g(-1) (wet weight) in Scomberomorus sierra to a low of 0.009 µg g(-1) in Catostomidae. Average Hg levels were within published toxicity threshold values in forage fish for only two sites in Mexico (Puerto Vallarta and San Blas Estuary), and all were marine species, such as mackerel (Scomberomorus sierra), sea catfish (Ariopus spp.), and sardinas species (Centropomus spp.). Except for one sample from Nicaragua, sea catfish from Puerto Morazan, none of the fish from sites in Central America had Hg levels which exceeded the thresholds. Nonmetric multidimensional scaling revealed geographical differences in Hg levels with significant pairwise differences between sites along the Pacific Ocean (Mexico) versus the Bay of Campeche, partly due to differences in species composition of sampled fish (and species distributions). Hg increased with trophic level, as assessed by nitrogen stable isotope ratios (δ(15)N but not δ(13)C), in freshwater and marine, but not estuarine, environments. Hg concentrations in forage fish do not account for the elevated Hg reported for many osprey populations on the breeding grounds, thus primary sources of contamination appear to be in the north.

Temporal trends of perfluoroalkyl substances (PFAS) in eggs of coastal and offshore birds: Increasing PFAS levels associated with offshore bird species breeding on the Pacific coast of Canada and wintering near Asia.

Perfluoroalkyl substances (PFAS) such as perfluoroalkyl carboxylates (PFCAs) and perfluoroalkyl sulfonates (PFSAs) have become virtually ubiquitous throughout the environment, and, based on laboratory studies, have known toxicological consequences. Various national and international voluntary phase-outs and restrictions on these compounds have been implemented over the last 10 to 15 years. In the present study, we examine trends (1990/1991-2010/2011) in aquatic birds (ancient murrelet, Synthliboramphus antiquus [2009 only]; Leach's storm-petrels, Oceanodroma leucorhoa; rhinoceros auklets, Cerorhinca monocerata; double-crested cormorants, Phalacrocorax auritus; and great blue herons, Ardea herodias). The PFCA, PFSA, and stable isotope (δ(15) N and δ(13) C) data collected from these species from the Pacific coast of Canada, ranging over 20 to 30 years, were used to investigate temporal changes in PFAS coupled to dietary changes. Perfluorooctane sulfonic acid (PFOS), the dominant PFSA compound in all 4 species, increased and subsequently decreased in auklet and cormorant eggs in line with the manufacturing phase-out of PFOS and perfluorooctanoic acid (PFOA), but concentrations continuously increased in petrel eggs and remained largely unchanged in heron eggs. Dominant PFCA compounds varied between the offshore and coastal species, with increases seen in the offshore species and little or variable changes seen in the coastal species. Little temporal change was seen in stable isotope values, indicating that diet alone is not driving observed PFAS concentrations.

PBDEs and other POPs in urban birds of prey partly explained by trophic level and carbon source.

As urban sprawl and agricultural intensification continue to invade prime wildlife habitat, some animals, even apex predators, are managing to adapt to this new environment. Chemical pollution is one of many stressors that wildlife encounter in urban environments. Predators are particularly sensitive to persistent chemical pollutants because they feed at a high trophic level where such pollution is biomagnified. To examine levels of pollution in urban birds of prey in the Lower Mainland region of British Columbia, Canada, we analyzed persistent organic contaminants in adult birds found dead of trauma injury. The hepatic geometric mean concentration of sum polybrominated diphenyl ethers (∑PBDEs) in 13 Cooper's hawks (Accipiter cooperii) from Greater Vancouver was 1873 ng/g (lipid weight) with one bird reaching 197,000n g/g lipid weight, the highest exposure reported to date for a wild bird. Concentrations of ∑PBDEs, ∑PCBs (polychlorinated biphenyls) and, surprisingly, cyclodiene insecticides were greatest in the urban environment while those of DDE (1,1-dichloroethylene bis[p-chlorophenyl) were highest in a region of intensive agriculture. The level of most chlorinated and brominated contaminants increased with trophic level (δ(15)N). The concentrations of some contaminants, PBDEs in particular, in these birds of prey may have some toxicological consequences. Apex predators in urban environments continue to be exposed to elevated concentrations of legacy pollutants as well as more recent brominated pollutants.

Brominated flame retardant trends in aquatic birds from the Salish Sea region of the west coast of North America, including a mini-review of recent trends in marine and estuarine birds.

Polybrominated diphenyl ethers (PBDEs) increased in many matrices during the 1990s and early 2000s. Since voluntary restrictions and regulations on PBDEs were implemented in North America circa early 2000s, decreases in PBDEs have occurred in many of these same matrices. To examine temporal trends in the North Pacific, we retrospectively analysed PBDEs and eight non-PBDE flame retardants (FR) in eggs of two aquatic bird species, great blue herons, Ardea herodias, and double-crested cormorants, Phalacrocorax auritus, collected along the British Columbia coast, Canada from 1979 to 2012. Increasing PBDE concentrations were observed in both species followed by significant decreases post-2000 for all dominant congeners and ΣPBDE. Non-PBDE FRs were generally undetected in cormorant eggs, or detected at very low levels in heron eggs, except for hexabromocyclododecane (HBCDD). HBCDD, currently unregulated in North America, was not detected in early sampling years; however low concentrations were observed in both species in recent sampling years (2003-2012). Dietary tracers (δ(13)C and δ(15)N) did not change significantly over time, indicating that temporal changes in PBDEs are likely caused by implemented regulations. A comparison with recently published temporal trends of ΣPBDE in marine birds from North America and Europe is given.

Spatial and temporal trends in brominated flame retardants in seabirds from the Pacific coast of Canada.

Polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecane (HBCDD) are bioaccumulative flame retardants. PBDEs increased in many ecosystems during the late 20th century, but recently have declined in some environments. To examine trends in the northern Pacific, we analysed PBDEs, HBCDD and carbon and nitrogen stable isotopes (δ13C and δ15N) to account for dietary effects in archived eggs of three seabird species from British Columbia, Canada, 1990-2011 (rhinoceros auklets, Cerorhinca monocerata; Leach's storm-petrels, Oceanodroma leucorhoa; ancient murrelets, Synthliboramphus antiquus, 2009 only). PBDEs increased until approximately 2000 and then decreased, while HBCDD increased exponentially throughout the examined period. No significant changes in dietary tracers were observed. HBCDD and ΣPBDE levels varied among species; ΣPBDE also varied among sites. Temporal changes in contaminant concentrations are unlikely to have been caused by dietary changes, and likely reflect the build-up followed by decreases associated with voluntary phase-outs and regulations implemented in North America to control PBDEs.