Variations in thyroid hormone levels in endangered St. Lawrence Estuary belugas: Potential linkage with stress and organohalogen contaminant exposure.

The St. Lawrence Estuary (SLE) beluga (Delphinapterus leucas) population is highly exposed to an array of contaminants that were identified as one of the causes to the non-recovery of this endangered and declining population. In the last decade, an increasing number of parturition-associated complications and calf mortality has been reported in this population. It was suggested that elevated exposure to organohalogens (e.g., the halogenated flame retardants polybrominated diphenyl ethers [PBDEs]) and stress could play a role in this phenomenon by perturbing thyroid hormones. The objective of this study was to investigate the impact of concentrations of organohalogen contaminants and stress (cortisol levels) on thyroid hormone variations in adult male and female SLE belugas. Because plasma could not be collected in SLE belugas for ethical reasons, skin biopsy (n = 40) was used as a less-invasive alternative matrix to determine organohalogens (PBDEs and other halogenated flame retardants, polychlorinated biphenyls, and organochlorine pesticides), cortisol, and thyroid hormones (triiodothyronine [T3] and thyroxine [T4]), and their metabolites reverse T3 and 3,5-diiodothyronine [3,5-T2]). Cortisol and thyroid hormones were analyzed by ultra-performance liquid chromatography-multiple reactions monitoring mass spectrometry (UPLC-MRM/MS). This method was compared using skin and plasma samples obtained from Arctic belugas. Comparisons of linear models showed that cortisol was a weak predictor for T4, rT3 and 3,5-T2. Specifically, there was a weak significant negative association between T4 and cortisol levels. Moreover, in male SLE belugas, a weak significant positive association was found between T3 and Σ34PBDE concentrations in skin. Our findings suggest that stress (i.e., elevated skin cortisol levels) along with organohalogen exposure (mainly PBDEs) may be associated with thyroid hormone level perturbations in skin of cetaceans.

Impact of landfill characteristics on the atmospheric exposure to halogenated flame retardants in gulls.

Large amounts of consumer products containing halogenated flame retardants (HFRs) are disposed of annually in landfills, which may lead to significant releases of these semi-volatile contaminants into the environment. During their foraging activities in landfills, gulls can be exposed to elevated levels of HFRs in air. Ring-billed gulls (Larus delawarensis) breeding in the densely populated Montreal area (QC, Canada) are significantly exposed to air levels of polybrominated diphenyl ethers (PBDEs) in or in the vicinity of landfills. However, no information is currently available on the specific characteristics of these landfills that can modulate the atmospheric exposure of ring-billed gulls to HFRs. The objective of this study was to investigate how atmospheric exposure in ring-billed gulls to PBDEs and other HFRs is influenced by selected landfill characteristics (i.e., daily cover materials, waste types and tonnage). Miniature passive air samplers (PASs) combined with GPS dataloggers were deployed for ten days during six years on the back of wild-caught ring-billed gulls breeding in the Montreal area. Atmospheric levels of several PBDEs and other HFRs determined in PASs were found to increase with the presence probability of gulls in the two largest landfills using automotive shredder residues as daily cover material. Weather variables including relative humidity and wind speed had a weak influence on atmospheric levels of HFRs in the bird-borne PASs. Our results suggest that automotive shredder residues represent a significant emission source of HFRs into the air of landfills, thus influencing atmospheric exposure of gulls and other birds foraging in these sites.

Halogenated flame retardant exposure pathways in urban-adapted gulls: Are atmospheric routes underestimated?

Urban-adapted gulls can be exposed to flame retardants while foraging in landfills where elevated concentrations of polybrominated diphenyl ethers (PBDEs) and other halogenated flame retardants (HFRs) have frequently been measured in air. However, the contribution of atmospheric exposure has largely been overlooked compared to dietary exposure in birds and other wildlife. The overall objective of this study was to investigate the contribution of atmospheric exposure pathways relative to diet for PBDEs and other HFRs in ring-billed gulls (Larus delawarensis) nesting in the densely populated Montreal area (QC, Canada). Miniature passive air samplers (PASs) were deployed on the back of wild-caught ring-billed gulls for ten days. Concentrations of PBDEs and other HFRs were determined in PASs carried by ring-billed gulls as well as their lungs, stomach content, liver, preen oil, and onto the surface of their feathers. We evaluated the atmospheric and dietary exposure routes for the most abundant HFRs in samples using a structural equation model implemented in a Bayesian framework. Results indicated that lung concentrations of BDE-28 increased with its levels in air determined using bird-borne PASs. No association was found between BDE-28 concentrations in lungs and liver, whereas BDE-209 concentrations in liver increased with those in lungs. Moreover, BDE-28 and -47 concentrations in liver increased with those on feather surface, while liver BDE-47 concentrations were also positively related with those in stomach content. These findings suggested that, in addition to dietary exposure, atmospheric exposure pathways through inhalation and co-ingestion during feather maintenance (preening) significantly contribute to the accumulation of PBDEs in liver of ring-billed gulls. Atmospheric exposure to HFRs should therefore be considered in future landfill-foraging wildlife species as a potential exposure route compared to the traditional dietary exposure pathway.

Biotransformation of Dec-604 and potential effect on thyroid deiodinase activity in highly flame retardant-exposed gulls.

Several halogenated flame retardants (HFRs) have been identified as thyroid disruptors in birds including the polybrominated diphenyl ether (PBDE) mixtures, which have been replaced with other HFRs such as Dechlorane-604 (Dec-604). Dec-604 Component B (Dec-604 CB), a putative debrominated product of Dec-604, has been frequently reported in urban-adapted ring-billed gulls (Larus delawarensis) breeding in the Montreal area (QC, Canada). The metabolic pathways of Dec-604 are yet to be characterized, although the occurrence of Dec-604 CB in gulls may suggest that enzyme-mediated dehalogenation may occur, potentially involving the thyroid deiodinases. The objective of this study was to investigate the effect of Dec-604 on type 1 deiodinase (DIO1) in the presence of thyroxine (T4) in an in vitro DIO1 assay using liver microsomes of ring-billed gulls that are highly exposed to HFRs in the Montreal area, and to determine whether DIO1 is involved in the in vitro debromination of Dec-604. We tested the in vitro activity of DIO1 in gull liver microsomes in the presence of five concentrations of Dec-604 ranging from 0.86 to 86.21 nM. HFR concentrations (Σ40HFR) were also determined in liver samples of gulls. Results showed that total DIO1 activity in gull liver microsomes was increased by three of the five concentrations of Dec-604. No relationship between liver Σ40HFR concentrations and DIO1 activity was observed, except for T2 formation rates that significantly decreased with increasing liver HFR concentrations. Moreover, greater Dec-604 CB to Dec-604 concentration ratios in activated gull microsomes (with the DIO1 cofactor dithiothreitol) were found at the intermediate Dec-604 concentration compared to controls. These results suggested that liver microsome DIO1 activity may be perturbed in ring-billed gulls exposed to Dec-604, and be involved at least in part, in the debromination of Dec-604 leading to the formation of Dec-604 CB.

Occurrence and temporal trends of industrial antioxidants and UV absorbents in the endangered St. Lawrence Estuary beluga whale (Delphinapterus leucas).

Elevated contaminant exposure has been identified as a stressor that has negative impacts on the health and recovery of the endangered St. Lawrence Estuary (SLE) beluga (Delphinapterus leucas) population. However, the accumulation of many groups of contaminants of emerging concern is still unknown in the SLE beluga. The objective of this study was to investigate the occurrence and temporal trends (2000-2017) of synthetic phenolic antioxidants (SPAs), secondary aromatic amines (Ar-SAs), benzotriazole UV stabilizers (BZT-UVs), and organic UV filters (UVFs) in the blubber (n = 69) and liver (n = 80) of SLE beluga carcasses recovered in the SLE. The SPA 2,6-di-tert-butyl-1,4-benzoquinone (BHTQ) was the most prevalent contaminant in the blubber (detection frequency: 86 %; median: 71.1 ng/g wet weight (ww)) and liver (50 %; 12.2 ng/g ww) of SLE belugas. In the blubber, 2-hydroxy-4-methoxybenzophenone (BP3) (36 %; 3.15 ng/g ww) and 2-(2H-benzotriazol-2-yl)-4-(1,1,3,3-tetramethyl butyl)phenol (UV329) (49 %; 6.84 ng/g ww) were the most frequently detected UVFs and BZT-UVs, respectively. Ar-SAs were not detected in most of the blubber and liver samples. Blubber accumulated higher levels of BHTQ and UV329 than liver, whereas the levels of BP3 were greater in the liver. Male SLE beluga accumulated greater concentrations of UV329 in blubber compared to females. These results indicated that the accumulation of BHTQ, UV329 and BP3 in SLE belugas is tissue- and sex-specific. BHTQ showed a decreasing trend in the blubber (2000-2017) of male SLE beluga, whereas no significant trend of this contaminant was found in females. UV329 showed no discernible temporal trend. This study established a baseline for the future monitoring of SPAs, Ar-SAs, BZT-UVs and UVFs in belugas and other marine mammals.

Triclosan is the Predominant Antibacterial Compound in Ontario Sewage Sludge.

Sewage treatment plants (STPs) accumulate both antibiotic and nonantibiotic antimicrobial compounds that can select for antibiotic resistant bacteria. Herein, we aimed to identify the predominant antibacterial compounds impacting E. coli from Ontario sewage sludge consisting of thousands of unknown compounds. Among the 10 extracted sludge samples, 6 extracts exerted significant growth inhibition effects in E. coli. A total of 103 compounds were tentatively detected across the 10 sludge samples by suspect screening, among which the bacterial enoyl-ACP reductase (FabI) inhibitor triclocarban was detected at the highest abundance. A hypomorphic FabI knockdown E. coli strain was highly susceptible to the sludge extracts, confirming FabI inhibitors as the primary antibacterial compounds in the sludge. Protein affinity pulldown identified triclosan as the major ligand binding to a His-tagged FabI protein from the sludge, despite the higher abundance of triclocarban in the same samples. Effect-directed analysis was used to determine the contributions of triclosan to the observed antibacterial potencies. Antibacterial effects were only detected in F17 and F18 across 20 fractions, which was consistent with the elution of triclosan and triclocarban in the same two fractions. Further, potency mass balance analysis confirmed that triclosan explained the majority (58-113%) of inhibition effects from sludge extracts. This study highlighted triclosan as the predominant antibacterial compound in sewage sludge impacting E. coli despite the co-occurrence of numerous other antibiotics and nonantibiotics.

Flame retardants and their associations with thyroid hormone-related variables in northern fulmars from the Faroe Islands.

Flame retardants (FRs) are widely reported in tissues of seabirds including birds sampled from remote areas. There is evidence that FRs can disrupt the hypothalamic-pituitary-thyroid (HPT) axis in seabirds, although information is limited on thyroid-related mechanisms and effects. This study investigated the associations between concentrations of polybrominated diphenyl ethers (PBDEs) and other FRs, and changes in the HPT axis in northern fulmars (Fulmarus glacialis) from the Faroe Islands (North Atlantic). Plasma concentrations of thyroid hormones (THs), hepatic deiodinase type 1 (D1) activity, and transcription of selected TH-related genes in liver were used as markers of HPT axis changes. Liver concentrations of a certain PBDE congeners and other FRs including pentabromoethylbenzene (PBEB), dechlorane 602 (Dec-602), and dechlorane plus (DP) were associated with changes in thyroid status. Specifically, liver PBDE, PBEB and Dec-602 concentrations were associated with plasma TH levels (free thyroxine [FT4] and total triiodothyronine [TT3]). Liver DP concentrations were positively correlated with the TT4:FT4 ratios and mRNA levels of UDP-glucuronyltransferase-1, while those of PBEB were negatively associated with TT4:TT3 ratios and D1 activity. D1 activity was also positively associated with the tri-, tetra- and hexa-BDE congeners. Moreover, transcription of ABCC2, a hepatic TH transporter, was associated with certain liver PBDE concentrations. Although PBDEs and other FRs may be potential inhibitors of D1 activity, only a few of the targeted FRs had modest associations with hepatic D1 activity. Regardless, the relationships reported herein indicated that exposure to moderate levels of FRs can be associated with thyroid axis perturbation at the molecular/biochemical levels in this North Atlantic seabird species.

Disruption by stealth - Interference of endocrine disrupting chemicals on hormonal crosstalk with thyroid axis function in humans and other animals.

Thyroid hormones (THs) are important regulators of growth, development, and homeostasis of all vertebrates. There are many environmental contaminants that are known to disrupt TH action, yet their mechanisms are only partially understood. While the effects of Endocrine Disrupting Chemicals (EDCs) are mostly studied as "hormone system silos", the present critical review highlights the complexity of EDCs interfering with TH function through their interactions with other hormonal axes involved in reproduction, stress, and energy metabolism. The impact of EDCs on components that are shared between hormone signaling pathways or intersect between pathways can thus extend beyond the molecular ramifications to cellular, physiological, behavioral, and whole-body consequences for exposed organisms. The comparatively more extensive studies conducted in mammalian models provides encouraging support for expanded investigation and highlight the paucity of data generated in other non-mammalian vertebrate classes. As greater genomics-based resources become available across vertebrate classes, better identification and delineation of EDC effects, modes of action, and identification of effective biomarkers suitable for HPT disruption is possible. EDC-derived effects are likely to cascade into a plurality of physiological effects far more complex than the few variables tested within any research studies. The field should move towards understanding a system of hormonal systems' interactions rather than maintaining hormone system silos.

Time-dependent biological responses of juvenile yellow perch (Perca flavescens) exposed in situ to a major urban effluent.

Municipal wastewater treatment plant (WWTP) effluents are significant sources of organic and inorganic pollutants to aquatic ecosystems. Several studies have shown that the health of aquatic organisms can be adversely impacted following exposure to these complex chemical mixtures. The objective of this study was to examine the effects of in situ exposure in the St. Lawrence River (QC, Canada) of juvenile yellow perch (Perca flavescens) to a major WWTP effluent. Perch were caged at a reference site in the St. Lawrence River and downstream of a WWTP effluent-influenced site for one, three, and six weeks. Fish kept in controlled laboratory setting were also examined at the beginning of the experiment to evaluate the potential effect of caging on fish. Liver metabolites and gill oxidative stress biomarkers as well as body condition of perch were investigated at four time points (zero, one, three, and six weeks). Nitrogen (δ15N) and carbon (δ13C) stable isotopes as well as tissue concentrations of halogenated flame retardants and trace metals were also analyzed. Results indicated that body condition of perch caged in the effluent increased after three and six weeks of exposure compared to that of reference fish. Perch caged at the WWTP effluent-influenced site also had higher muscle δ13C and slightly depleted muscle δ15N after three and six weeks of exposure, suggesting differences in sewage-derived nutrient assimilation between sites. Concentrations of Σ34 polybrominated diphenyl ether (PBDE) were 2-fold greater in perch exposed downstream of the WWTP compared to those caged at the reference site. Metal concentrations in kidney of perch after three weeks of exposure were significantly lower at the effluent-influenced site. Kidney concentrations of Cd, Cu, Se, As, Zn and Fe were, however, higher after six weeks of exposure, supporting that metal accumulation is time- and element-specific. The metabolomes of perch from the effluent-influenced and reference sites were similar, but were distinct from the laboratory control fish, suggesting a caging effect on fish. Seven liver metabolites (glucose, malate, fumarate, glutamate, creatinine, histamine, and oxypurinol) were significantly more abundant in perch from cages than in the laboratory control perch. The combination of metabolomics and physiological variables provides a powerful tool to improve our understanding of the mechanisms of action of complex environmental pollutant mixtures in wild fish.

Spatial and temporal variations of halogenated flame retardants and organophosphate esters in landfill air: Potential linkages with gull exposure.

Landfills represent important sources of local emissions of organic contaminants, including halogenated (HFR) and organophosphate ester (OPE) flame retardants used in a large variety of consumer products. Gulls foraging in landfills may be exposed to elevated atmospheric concentrations of HFRs and OPEs that may vary spatially and temporally within a landfill site, thus modulating their exposure. The objective of the present study was to investigate the spatial and temporal variability of HFR and OPE concentrations in air samples collected from a major landfill in the Montreal area (QC, Canada) that is frequently visited by gulls for foraging. Miniature stationary passive air samplers (PASs) and high-volume active air samplers (AASs) were deployed in six different areas within this landfill site for 34 days to collect HFRs and OPEs in air. During the same period, wild-caught ring-billed gulls (Larus delawarensis) were equipped on their back with a similar miniature PAS that was deployed in the landfill along with a GPS datalogger to monitor their movements for ten days. Elevated concentrations of certain OPEs (e.g., tris(2-chloroethyl) phosphate and tris(2-chloroisopropyl) phosphate) and brominated diphenyl ether (BDE)-209 were measured in stationary PASs and AASs, although they were homogenously distributed within this landfill site. Temporal variability was observed for concentrations of BDE-209, -99 and -47 measured in AASs as well as tributyl phosphate during the 34-day deployment period. Moreover, air concentrations of BDE-209, -207 and -206 and selected OPEs (tris(1,3-dichloro-2-propyl) phosphate and tris(methylphenyl) phosphate) determined using AASs were positively correlated with ambient air temperatures. Gulls that visited a landfill at least once exhibited significantly greater concentrations of BDE-47 measured in PASs they carried on their back, suggesting that landfill air may represent a source of exposure to PBDEs for these birds, and potentially other urban-adapted wildlife using these sites for foraging.

Suspect and Nontarget Screening Revealed Class-Specific Temporal Trends (2000-2017) of Poly- and Perfluoroalkyl Substances in St. Lawrence Beluga Whales.

The global use of >3000 per- and polyfluoroalkyl substances (PFASs) has given rise to chemical regulatory action. However, limited information exists regarding current and historical emissions for the majority of PFASs under currently implemented regulations. This study employed suspect and nontarget screening to examine the temporal trends of legacy and unregulated PFASs in liver of the endangered beluga whale (Delphinapterus leucas) population from the St. Lawrence Estuary in Canada collected from 2000 to 2017. A suite of 54 PFASs were tentatively identified, and were grouped into nine structurally distinct classes. Single-hydrogenated perfluoro carboxylic acids (H-PFCAs), single-hydrogenated sulfonamides (H-Sulfonamides), as well as other select sulfonamides were detected for the first time in wildlife. Greater concentrations of the majority of PFASs were determined in newborns and juveniles than in adults, suggesting effective placental and lactational transfer of PFASs. Legacy per- and polyfluoroalkyl acids and perfluorooctane sulfonamide in beluga whale liver were found to significantly decrease in concentration between 2000 and 2017, while unregulated short-chain PFAS alternatives, H-PFCAs, and odd-chain FTCAs were found to increase over time. The implementation of suspect and nontarget screening revealed class-specific temporal trends of PFASs in SLE beluga whales, and supported continuous emissions of unregulated PFASs into the environment.

Gulls foraging in landfills: Does atmospheric exposure to halogenated flame retardants result in bioaccumulation?

Several bird species have adapted to foraging in landfills, although these sites are known to represent significant sources of emissions of toxic semi-volatile chemicals including the halogenated flame retardants (HFRs) (e.g., polybrominated diphenyl ethers (PBDEs) and emerging compounds). The objective of this study was to investigate the association between atmospheric exposure to PBDEs and selected emerging HFRs and their bioaccumulation in landfill-foraging birds. We determined HFR concentrations in liver of 58 GPS-tagged ring-billed gulls (Larus delawarensis) breeding in a colony near Montreal (Canada) as well as their atmospheric exposure determined using a miniature bird-borne passive air sampler. PBDE mixtures were the most abundant HFRs determined in passive air samplers (daily exposure rates of ∑9PentaBDE: 47.4 ± 6.5 pg/day; DecaBDE: 36.0 ± 6.3 pg/day, and ∑3OctaBDE: 3.4 ± 0.5 pg/day) and liver (∑9PentaBDE: 68.1 ± 8.9 ng/g ww; DecaBDE: 52.3 ± 8.1 ng/g ww, and ∑3OctaBDE: 12.8 ± 2.1 ng/g ww), and their concentrations increased with the presence probability of gulls in landfills. We found a spatial relationship between the local sources of atmospheric exposure to PBDEs and the sites associated with greatest PBDE concentrations in liver. Specifically, the atmospheric exposure index was correlated with the bioaccumulation index (Pearson r for ∑9PentaBDE: r = 0.63, p < 0.001; DecaBDE: r = 0.66, p < 0.001, and ∑3OctaBDE: r = 0.42, p < 0.001). However, we found no correlation at the individual level between daily exposure rates of HFRs in passive air samplers and their liver concentrations. This suggests that complex exposure pathways combined with toxicokinetic factors shaped HFR profiles in gull liver, potentially confounding the relationships with atmospheric exposure.

Lipid metabolites as indicators of body condition in highly contaminant-exposed belugas from the endangered St. Lawrence Estuary population (Canada).

The endangered St. Lawrence Estuary (SLE) beluga population is declining and has shown no sign of recovery over the past decades despite several protective measures. Changes in the availability of food resources and exposure to organohalogen contaminants have been suggested as potential factors limiting the recovery of this population. Studies on SLE belugas have suggested that contaminant exposure may perturb energy metabolism, however, whether this translates into changes in energy reserves (lipid composition) and body condition is unknown. The objective of this study was to investigate the relationships between body condition and concentrations of organohalogens (polychlorinated biphenyls, organochlorine pesticides, and flame retardants) and a range of lipid metabolites (fatty acids, acylcarnitines, lysophosphatidylcholines, phosphatidylcholines, and sphingomyelins) in blubber samples collected from 51 SLE beluga carcasses recovered between 1998 and 2016 for which the cause of mortality was documented. Blubber Σ9fatty acid concentrations in SLE belugas significantly decreased between 1998 and 2016, suggesting a decline in energy reserves over the past two decades. Concentrations of several phosphatidylcholine analogues were greater in blubber of beluga males and/or females that were in poor body condition compared to those in good body condition. Moreover, concentrations of phosphatidylcholine acyl-alkyl C32:2 were greater in females that died from primary starvation (poor body condition). Greater concentrations of Σ12emerging flame retardants were also found in blubber of SLE beluga females that were in poorer body condition. This study suggests that the use of membrane lipids including phosphatidylcholine concentrations may be a good indicator of body condition and energy reserve status in blubber of marine mammals.

Trophic transfer of polybrominated diphenyl ethers in a recently modified freshwater food web from the St. Lawrence River, Canada.

Introduction of invasive species can have a profound impact on food web structure and therefore on trophic transfer of contaminants. In the St. Lawrence River (Canada), 20 years after its first detection in the system, invasive round goby (Neogobius melanostomus) has become the main prey for several piscivorous species. To evaluate the accumulation, trophic transfer, and the ecological risk of polybrominated diphenyl ethers (PBDEs) in this recently modified freshwater food web, samples of sediment, invertebrates, fish and aquatic bird eggs and plasma were collected. Sampling sites were located upstream and at two locations downstream of the Montreal wastewater treatment plant outfall. The results suggest that the influence of the WWTP effluent on PBDEs concentrations varied among the various compartments of this recently modified freshwater food web. The results also suggest that although predatory fish have switched to consuming round goby as a prey item instead of native yellow perch, this new feeding behaviour is not expected to have important impacts on the level of transfer of PBDE within this food web. The biota-sediment accumulation factors (BSAFs) ranged from 0.6 to 436, whereas biomagnification factors (BMFs) varied between 0.2 and 475. Despite our conservative method of risk assessment, we calculated an important risk for piscivorous fish and gull eggs within this study area.

Bidirectional transfer of halogenated flame retardants between the gastrointestinal tract and ingested plastics in urban-adapted ring-billed gulls.

The hypothesis that plastics can transfer chemical pollutants to organisms after ingestion has been supported by several lab and field studies. However, models indicate that this transfer could be bidirectional and that whether chemicals move from plastics to the animal or vice versa, depends on several factors, including the relative concentrations of chemicals in both the animal and the plastics ingested. To explore this phenomenon in the field, we examined the relative concentrations of several halogenated flame retardants (HFRs) in a population of urban-dwelling ring-billed gulls (Larus delawarensis) and the plastics in their gastrointestinal (GI) tracts. We predicted the direction of transfer for HFRs between these birds and their ingested plastics using assumptions based on equilibrium theory. Because we were also interested in the sources of ingested plastics in this population, we investigated the relationships between time spent in different foraging habitats (determined using GPS-based telemetry) and the amounts and morphologies of plastics in their GI tracts. Results suggest that for this highly HFR-exposed population of ring-billed gulls, chemical transfer between plastics and bird is bidirectional, with a dominance of transfer from bird to ingested plastics. We also observed a relationship whereby birds that ingested no or low amounts of plastics were most closely associated with the use of residential habitats. Overall, we conclude that whether ingested plastics is a source or sink of chemicals to organisms is a complex and context-dependent phenomenon, and likely varies based on parameters such as exposure level and feeding ecology.

An investigation of physiological effects of the Deepwater Horizon oil spill on a long-distance migratory seabird, the northern gannet.

Exposure to oil can have long-term impacts on migratory birds. Following the 2010 Deepwater Horizon blowout in the Gulf of Mexico (GOM), we investigated potential impacts of oil exposure on a population of northern gannets (Morus bassanus) that breed on Bonaventure Island (Québec, Canada) and winter in GOM and along the U.S. Atlantic coast (AC). Blood and feather samples were collected from adults previously equipped with geolocators to determine wintering locations. Parent and alkylated polycyclic aromatic hydrocarbons (PAHs); trace metals; stable isotopes of carbon, nitrogen, and hydrogen; and immune, thyroid, steroid, retinoid, and genetic endpoints were measured. PAH and trace metal concentrations did not differ between gannets using different wintering sites. Feather stable isotope values varied significantly between birds from different wintering locations. Gannets wintering in GOM showed higher feather corticosterone and plasma thyroid hormone levels, which may indicate increased energetic demands and/or greater exposure to environmental stressors.

Metabolomic profiles of the endangered St. Lawrence Estuary beluga population and associations with organohalogen contaminants.

The endangered beluga (Delphinapterus leucas) population residing in the St. Lawrence Estuary (SLE; Eastern Canada) is declining. The elevated tissue concentrations of a wide range of organohalogen contaminants might play a role in the non-recovery of this whale population. Organohalogens have been reported to impair the regulation of several metabolic products from cellular reactions in mammals such as amino acids and fatty acids. The objective of this study was to investigate a suite of organohalogens including polychlorinated biphenyls, organochlorine pesticides, short-chain chlorinated paraffins (SCCPs), polybrominated diphenyl ethers, and selected emerging flame retardants in blubber (biopsy) collected from 40 SLE male belugas, and their relationships to skin concentrations of targeted metabolites (i.e., 21 amino acids, 22 biogenic amines, 18 fatty acids, and 17 energy metabolites). A cluster analysis based on metabolomic profiles distinguished two main subgroups of belugas in the upper and lower sector of their summer habitat in the SLE. These results indicate that ecological factors such as local prey availability and diet composition played a role in shaping the metabolite profiles of belugas. Moreover, SCCP concentrations in SLE male belugas correlated negatively with those of four unsaturated fatty acids (C16:1ω7, C22:5ω3c1, C22:5ω3c2, and C22:6ω3), and positively with those of acetylornithine (biogenic amine). These findings suggest that biological functions such as lipid metabolism represent potential targets for organohalogens in this population, and further our understanding on potential health risks associated with elevated organohalogen exposure in cetaceans. Our results also underscore the necessity of considering ecological factors (e.g., diet and habitat use) in metabolomic studies.

Environmental exposure of northern pike to a primary wastewater effluent: Impact on the lipidomic profile and lipid metabolism.

Lipids play important roles in growth, reproduction, locomotion, and migration of fish. Municipal effluents, which are complex mixtures of biological and chemical compounds including flame retardants, have been shown to alter lipid metabletabolism in environmentally and experimentally exposed fish. Down-regulation of several genes coding for fatty acid metabolism enzymes has previously been reported in male northern pike (Esox lucius) collected in the St. Lawrence River (QC, Canada) downstream of a major primary wastewater treatment plant (WWTP) point of discharge. The main objective of this study was to investigate the effects of exposure to the Montreal's WWTP effluent on the lipidomic profile (i.e., fatty acids, acylcarnitines, and phospholipids) as well as the transcription of genes related to lipid metabolism in the liver of northern pike collected upstream and downstream of this WWTP effluent. Halogenated flame retardant concentrations were also determined in pike liver and used as markers of exposure to this effluent. Greater concentrations of saturated and monounsaturated lysophosphatidylcholines (LPCs) and lower concentrations of polyunsaturated LPCs were determined in the liver of pike collected downstream of the WWTP compared to those collected upstream. Lower mRNA levels of peroxisome proliferator-activated receptor alpha (pparα), a major regulator of lipid metabolism, were also measured in pike exposed to Montreal's WWTP effluent. In addition, the relative contributions (%) of LPC 18:2 and LPC14:0, compounds used as markers of obesity and inflammation, were significantly correlated with halogenated flame retardant concentrations and fish girth. Results of the present study suggest that chronic environmental exposure to a primary WWTP effluent can modulate the transcription of genes related to lipid metabolism, and hence affect the hepatic phospholipid composition of pike from the St. Lawrence River.

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.

Landfills represent significant atmospheric sources of exposure to halogenated flame retardants for urban-adapted gulls.

Halogenated flame retardants (HFRs) are contaminants that are abundantly emitted from waste management facilities (WMFs) and that became ubiquitous in air of urbanized regions. Urban birds including gulls have adapted to exploiting human food resources (refuse) in WMFs, and have thus experienced population explosions worldwide. However, foraging in WMFs for birds may result in exposure to HFRs that have been shown to be toxic for animals. The objective of this study was to determine the influence of foraging near or in various WMFs on the atmospheric exposure of birds to HFRs, and to localize other sources of HFRs at the regional scale in a highly urbanized environment. We measured the atmospheric exposure to HFRs in one of the most abundant gull species in North America, the ring-billed gull (Larus delawarensis), breeding in the densely-populated Montreal area (Canada) using a novel approach combining bird-borne GPS dataloggers and miniature passive air samplers (PASs). We determined concentrations of 11 polybrominated diphenyl ethers (PBDEs) and three emerging HFRs of high environmental concern in PASs carried by gulls. We show that the daily sampling rates (pg/day) of PBDEs in PASs were highest in gulls foraging in or around landfills, but were not influenced by meteorological variables. In contrast, the daily sampling rates of emerging HFRs were lower compared to PBDEs and were not influenced by the presence of gulls in or near WMFs. This study demonstrates that atmospheric exposure to HFRs and perhaps other semi-volatile contaminants is underestimated, yet important for birds foraging in landfills.