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.

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.

Northern fulmars as biological monitors of trends of plastic pollution in the eastern North Pacific.

Marine plastic debris is a global issue, which highlights the need for internationally standardized methods of monitoring plastic pollution. The stomach contents of beached northern fulmar (Fulmarus glacialis) have proven a cost-effective biomonitor in Europe. However, recent information on northern fulmar plastic ingestion is lacking in the North Pacific. We quantified the stomach contents of 67 fulmars from beaches in the eastern North Pacific in 2009-2010 and found that 92.5% of fulmars had ingested an average of 36.8 pieces, or 0.385 g of plastic. Plastic ingestion in these fulmars is among the highest recorded globally. Compared to earlier studies in the North Pacific, our findings indicate an increase in plastic ingestion over the past 40 years. This study substantiates the use of northern fulmar as biomonitors of plastic pollution in the North Pacific and suggests that the high levels of plastic pollution in this region warrant further monitoring.

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.

Anticoagulant rodenticides in three owl species from Western Canada, 1988-2003.

Anticoagulant rodenticides are widely used to control rodent infestations. Previous studies have shown that nontarget organisms, such as birds, are at risk for both primary and secondary poisoning. This paper presents rodenticide residue information on the livers from 164 strigiformes which included barn owls (Tyto alba), barred owls (Strix varia), and great horned owls (Bubo virginianus), collected from 1988 to 2003 in the province of British Columbia and the Yukon Territory, Canada. Livers were analyzed for brodifacoum, bromadiolone, chlorophacinone, diphacinone, difethialone, and warfarin. Our results show that, of the 164 owl livers analyzed, 70% had residues of at least one rodenticide, and of these 41% had more than one rodenticide detected. Of the three species of owls examined, barred owls were most frequently exposed (92%, n = 23); brodifacoum and bromadiolone were most often detected, with liver concentrations ranging from 0.001 to 0.927 mg/kg brodifacoum, and 0.002 to 1.012 mg/kg bromadiolone. Six of the owls (three barred owls, two barn owls, and one great horned owl) were diagnosed as having died from anticoagulant poisoning; all six owls had brodifacoum residues in the liver.

Fonofos poisons raptors and waterfowl several months after granular application.

From 1994 to 1999 in the Lower Fraser Valley region of southwest Canada, fonofos (Dyfonate G) was recommended for control of introduced wireworm (Agriotes spp.) pests on potato and other root crops. As part of a wildlife-monitoring program, we collected 15 raptors, including 12 bald eagles (Haliaeetus leucocephalus), found dead or debilitated on or near agricultural lands with severely inhibited brain and/or plasma cholinesterase activity and fonofos residues in ingesta. Bird remains, in nine cases waterfowl, were identified in the ingesta samples. Another seven bald eagles had severe cholinesterase inhibition, but without evidence of fonofos residues. During two winters from 1996 to 1998, 420 ha of potato fields, half of which had been treated the previous spring with fonofos and the remainder untreated, were searched weekly for evidence of wildlife mortality. Search efficiency was assessed with placed duck carcasses. Waterfowl outnumbered other species in field-use counts and comprised the greatest proportion of birds found dead. We found 211 wildlife remains, most scavenged; 35 intact carcasses were suitable for postmortem examination and/or toxicology analyses. Cholinesterase activity was assayed in brains of 18 waterfowl, five of which had severely depressed activity (average inhibition 74%; range, 69-78%). The gastrointestinal tract of a mallard found in a field treated with granular product contained 49 microg/g fonofos residues, linking waterfowl mortality with labelled use of the product. These findings demonstrate the risk of both primary and secondary poisoning by anticholinesterase insecticides where wildlife make intensive use of farmed fields.

The effects of environmental exposure to DDT on the brain of a songbird: changes in structures associated with mating and song.

Dichlorodiphenyltrichloroethane (DDT) is a persistent organochlorine compound found worldwide that causes significant anatomical, physiological and behavioural abnormalities in humans and wildlife. However, little is known about whether environmental exposure to DDT affects the brain. Here, we show that environmental exposure to DDT alters the brains of American Robins (Turdus migratorius) in several ways. Increasing levels of DDT resulted in: (i) smaller brain and relative forebrain volumes; (ii) a reduction in the size of two song nuclei, nucleus robustus arcopallialis (RA) and HVC; and (iii) a drastic reduction in neuronal size and overall volume of nucleus intercollicularis (ICo), a structure that is critical for normal sexual behaviour. These changes likely result from stress, direct neurotoxicity and androgen receptor antagonism by the primary metabolite of DDT, p,p'-DDE and this is corroborated by analyses of brain region volumes and p,p'-DDE levels. Our results therefore demonstrate that environmental exposure to DDT is correlated with significant changes in the brain and specifically those structures related to mating and song. Given the magnitude of these changes in the brain and the fact that environmental DDT exposure was restricted to early development, we conclude that both humans and wildlife that live in DDT contaminated environments may be at risk of neurological damage.

An assessment of PCBs and OC pesticides in eggs of double-crested (Phalacrocorax auritus) and Pelagic (P. pelagicus) cormorants from the west coast of Canada, 1970 to 2002.

Eggs of double-crested and pelagic cormorants were collected between 1970 and 2002 from colonies in the Strait of Georgia, BC, Canada, and assayed for concentrations of organochlorine (OC) pesticides and polychlorinated biphenyls (PCBs). Double-crested cormorant eggs from the early 1970's contained up to 4.1 mg kg-1 p,p'-DDE and 12.5 mg kg-1 sigmaPCBs. Corresponding values for pelagic cormorant eggs were 1.5 mg kg-1 p,p'-DDE and 3.9 mg kg-1 sigmaPCBs. Egg tissue concentrations of the dominant OC pesticides and sigmaPCBs dropped mainly during the 1970's, with minor declines thereafter. The data suggest that contaminant levels in cormorants have now stabilized at low levels throughout the resident population. Small but significant latitudinal gradients in several OC pesticides and PCBs indicated that areas of the southern strait were more contaminated than areas of the less populated northern strait. Interspecific differences in contamination may indicate that pelagic cormorants have a reduced capacity to metabolize chlordanes, DDT and PCBs compared to double-crested cormorants. Alternatively, the two species may have more divergent prey bases than previously thought. During the 1980's, TCDD toxic equivalents, largely contributed by polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs), were correlated with physiological and biochemical alterations. Also, from 1989 to 1990, four deformed cormorant chicks (two of each species) were found during nest visits; none were found between 1991 and 1995. The relative rates of deformed chicks were 6 per 10,000 for double-crested and 16 per 10,000 for pelagic cormorants. The findings of deformed chicks were coincident with the period of highest PCDD and PCDF contamination; however, the sample sizes were too low to derive a substantive connection. Colony-wide productivity of double-crested cormorants was poorer in the southern colonies where PCBs in particular were elevated. While of concern, these lines of evidence are insufficient to conclude that chlorinated hydrocarbon contamination was a dominant contributor to population declines. It seems more probable that ecological variables, particularly changing prey and predator dynamics, drove the reductions in population size.

Polybrominated diphenyl ether trends in eggs of marine and freshwater birds from British Columbia, Canada, 1979-2002.

Temporal, spatial, and interspecific trends in polybrominated diphenyl ether (PBDE) flame retardants were determined in eggs of marine and freshwater bird species from the province of British Columbia, Canada. Temporal trends in the Fraser River estuary, 1983-2002, were examined by analysis of eggs of great blue herons (Ardea herodias) and from the Strait of Georgia marine ecosystem, 1979-2002, in eggs of double-crested cormorants (Phalacrocorax auritus). Results were compared to those from eggs of the osprey (Pandion haliaetus) taken along the lower Fraser River and along the Columbia River near Castlegar, British Columbia, and of a pelagic seabird, the Leach's storm-petrel (Oceanodroma leucorhoa), collected at a colony on the Queen Charlotte Islands. Mean concentration of sigmaPBDE, 455 microg/kg w.w., were highest in heron eggs collected in 2002 from the Fraser estuary. Concentrations in eggs of cormorants and ospreys taken from sites of varying urban influence tended to be about half that value. Leach's storm petrel eggs had only trace amounts of sigmaPBDE (3.38 microg/kg), despite having similar concentrations of PCBs and organochlorine pesticides to the other species. PBDEs increased exponentially with a doubling time of 5.7 years in eggs of both herons and cormorants. Over this period of increasing PBDEs, major chlorinated hydrocarbons, such as PCBs and DDE, were stable or decreased. The PBDE pattern was relatively consistent in most years and sites, with BDEs 47 > 100 > 99 > 153 > 154 > 28 > 183. This was interpreted as evidence of technical pentaBDE formulations as primary sources of the contamination, with the octaBDE formulations as secondary. Higher resolution analysis of a subsample of the eggs revealed the presence of up to nine other congeners, including BDE209 (range: 0.9-1.8 microg/kg), indicating exposure and uptake of decaBDE sourced congeners in North American foodchains. At some locations, concentrations of pentabrominated congeners and mixtures in fish are approaching levels potentially toxic to fish-eating birds, based on rodent studies and calculations of dietary intake from fish data.

An assessment of DDT and other chlorinated compounds and the reproductive success of American robins (Turdus migratonrius) breeding in fruit orchards.

Although DDT was banned in the 1970s, American robins (Turdus migratorius) breeding in fruit orchards of the Okanagan Valley, British Columbia, continue to be contaminated with DDT and its metabolites. The objectives of our study were (1) to assess organochlorine (OC) contamination in robins breeding in Okanagan orchards (1993-1995, 1997-1998) and (2) to determine if exposure affected reproductive success when compared to robins from non-orchard habitat (lower mainland, British Columbia). Robins in orchards had total DDT egg residues of 48.64 mg/kg (geometric mean; n = 92) while those in non-orchard habitat had 1.10 mg/kg (geometric mean; n = 26), wet weight. The probability of nest survival during the incubation period was 96.7% (confidence interval: 95.7-97.5%; n = 165) in orchard habitat and 96.7% (confidence interval: 94.6-98.1%; n = 28) in non-orchard habitat. During the nestling period the probability of nest survival was 98.2% (confidence interval: 97.2-98.9%; n = 123) in orchard habitat and 96.2% (confidence interval: 92.8-98.0%; n = 34) in non-orchard habitat. Clutch (p < 0.0001) and brood size (p = 0.0133) were larger in orchards (n = 150 and n = 93, respectively) compared to non-orchard nests (n = 42 and n = 23, respectively) with no difference in fledge rate. DDE (r2 = 0.11, p = 0.0030, n = 68) and dieldrin (r2 = 0.29, p < 0.0001, n = 68) were negatively correlated with fledge rate in robin eggs collected from orchard habitat, however, low r2 values signify minimal biological significance. Although American robins nesting in Okanagan orchards are exposed to high OC levels, reproductive success does not appear to be negatively impacted.

Egg concentrations of polychlorinated dibenzo-p-dioxins and dibenzofurans in double-crested (Phalacrocorax auritus) and pelagic (P. pelagicus) cormorants from the Strait of Georgia, Canada, 1973-1998.

Eggs of double-crested and pelagic cormorants were collected between 1973 and 1998 from colonies in the Strait of Georgia, BC, Canada, and assayed for concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and non-ortho- and mono-ortho-biphenyls (PCBs). Double-crested cormorant eggs contained (on average) up to 433 ng kg(-1) wet weight 1,2,3,6,7,8-HxCDD, 151 ng kg(-1) 1,2,3,7,8-PnCDD, and 74 ng kg(-1) 2,3,7,8-TCDD, whereas pelagic cormorant eggs contained up to 300, 99, and 28 ng kg(-1) wet weight of these respective congeners. The dominant non-ortho-PCB was CB-126, which ranged as high as 2263 ng kg(-1) in double-crested cormorant eggs. Concentrations of PCDDs and PCDFs fell dramatically in the early 1990s, following both severe restrictions on the use of chlorophenolic wood preservatives and antisapstains and a switch from molecular chlorine bleaching to alternative bleaching technologies at pulp mills in the region. Concentrations of PCBs did not show similar marked declines over time. On the basis of total TEQs > or = 148 ng kg(-1) and previously published documentation of effects in siblings of the cormorant eggs analyzed here, double-crested cormorant young may have exhibited significantly elevated EROD activity and/or brain asymmetries at all colonies from 1973 to 1989 and even at some colonies during the 1990s. Pelagic cormorant eggs collected from a few colonies in 1988-1989 also contained total TEQs greater than the threshold value estimated for double-crested cormorants.

Persistence and retention of active ingredients in four granular cholinesterase-inhibiting insecticides in agricultural soils of the lower Fraser River valley, British Columbia, Canada, with implications for wildlife poisoning.

The persistence and retention of active ingredients in granules of Thimet 15G (phorate 15% by weight), Dyfonate 10G (fonofos 10% by weight), Counter 15G (terbufos 15% by weight), and Furadan 10G (carbofuran 10% by weight) were determined in silt loam and organic muck agricultural soils typical of the lower Fraser River valley (BC, Canada). In June 1995, treatment bags made of polyester cloth (7.5 x 7.5 cm) containing granules of a single insecticide, either alone or with soil, were placed during spring planting in the bottom of the furrow and retrieved periodically until April 1996. The parent component of each insecticide declined monotonically except for carbofuran (logistic decline). In the silt loam (organic muck) soil, the average June-to-October first-order rate constants and half-lives were 0.009 (0.010)/d and 80 (71) d for fonofos, 0.012 (0.009)/d and 58 (82) d for phorate, and 0.032 (0.015)/d and 21 (47) d for terbufos; the half-life of carbofuran was 129 (97) d. By December, the average amounts of fonofos and phorate in silt loam (organic muck) were 26% (range: 17-40%; 14% [range: 3.4-21%]) and 21% (range: 15-30%; 10% [range: 5.0-24%]) of the initial amounts of active ingredients measured at time zero, respectively. By April, the percentages dropped to 16% (range: 7.8-24%; 2.3% [range: 0-7.7%]) and 7.3% (range: 1.9-25%; 0.6% [range: 0-1.9%]). During this period, about 95% of the active ingredients were granule bound, the rest remaining in the bag. Only low levels of terbufos and carbofuran persisted in both soils from December to April of the following year. Results indicate an enhanced probability for poisoning of waterfowl and raptors because of the high levels of active ingredients retained on granules of all four insecticides in both soils in the fall. The risk of acute poisoning by phorate and fonofos continued though the winter.