Transcriptomic and developmental effects of persistent organic pollutants in sentinel fishes collected near an arctic formerly used defense site.

Alaska contains over 600 formerly used defense (FUD) sites, many of which serve as point sources of pollution. These sites are often co-located with rural communities that depend upon traditional subsistence foods, especially lipid-rich animals that bioaccumulate and biomagnify persistent organic pollutants (POPs). Many POPs are carcinogenic and endocrine-disrupting compounds that are associated with adverse health outcomes. Therefore, elevated exposure to POPs from point sources of pollution may contribute to disproportionate incidence of disease in arctic communities. We investigated PCB concentrations and the health implications of POP exposure in sentinel fishes collected near the Northeast Cape FUD site on Sivuqaq (St. Lawrence Island), Alaska. Sivuqaq residents are almost exclusively Yupik and rely on subsistence foods. At the request of the Sivuqaq community, we examined differential gene expression and developmental pathologies associated with exposure to POPs originating at the Northeast Cape FUD site. We found significantly higher levels of PCBs in Alaska blackfish (Dallia pectoralis) collected from contaminated sites downstream of the FUD site compared to fish collected from upstream reference sites. We compared transcriptomic profiles and histopathologies of these same blackfish. Blackfish from contaminated sites overexpressed genes involved in ribosomal and FoxO signaling pathways compared to blackfish from reference sites. Contaminated blackfish also had significantly fewer thyroid follicles and smaller pigmented macrophage aggregates. Conversely, we found that ninespine stickleback (Pungitius pungitius) from contaminated sites exhibited thyroid follicle hyperplasia. Despite our previous research reporting transcriptomic and endocrine differences in stickleback from contaminated vs. reference sites, we did not find significant differences in kidney or gonadal histomorphologies. Our results demonstrate that contaminants from the Northeast Cape FUD site are associated with altered gene expression and thyroid development in native fishes. These results are consistent with our prior work demonstrating disruption of the thyroid hormone axis in Sivuqaq residents.

Formerly used defense sites on Unalaska Island, Alaska: Mapping a legacy of environmental pollution.

Unalaska Island, Alaska, served as a US military base during World War II. The military installed bases on Unalaska and nearby islands, many of which were built adjacent to Unangan communities. The military used toxic compounds in its operations and left a legacy of pollution that may pose health risks to residents and local wildlife. The goals of this study were to identify hotspots of contamination remaining at Unalaska formerly used defense (FUD) sites, evaluate the risk posed by arsenic, and examine "no US Department of Defense action indicated" (NDAI) status determinations for FUD sites near communities. We compiled soil chemistry data from remediation reports prepared by the US Army Corps of Engineers at 18 FUD sites on and near Unalaska. Nine had past and/or active remediation projects and on-site sampling data. Eight sites did not have sampling data and were characterized as NDAI. One site was listed as closed. For the nine sites with sampling data, we compiled data for 22 contaminants of concern (COC) and compared concentrations to soil cleanup levels for human health (18 AAC 75.341). We mapped contaminant concentrations exceeding these levels to identify hotspots of contamination. We found that concentrations of some of the 22 COC exceeded Alaska cleanup levels despite remediation efforts, including diesel range organics, arsenic, and lead. The highest COC concentrations were at the FUD site adjacent to the City of Unalaska. A quantitative risk assessment for arsenic found that the risk of exposure through drinking water is low. We highlight concerns with NDAI designations and current remedial practices at remote FUD sites located adjacent to communities. Our data suggest the need for further remediation and monitoring efforts on Unalaska for certain contaminants and research to examine potential threats to human and animal health associated with these sites. Integr Environ Assess Manag 2024;00:1-12. © 2024 SETAC.

Differential gene expression and developmental pathologies associated with persistent organic pollutants in sentinel fish in Troutman Lake, Sivuqaq, Alaska.

Persistent organic pollutants (POPs) are lipophilic compounds that bioaccumulate in animals and biomagnify within food webs. Many POPs are endocrine disrupting compounds that impact vertebrate development. POPs accumulate in the Arctic via global distillation and thereby impact high trophic level vertebrates as well as people who live a subsistence lifestyle. The Arctic also contains thousands of point sources of pollution, such as formerly used defense (FUD) sites. Sivuqaq (St. Lawrence Island), Alaska was used by the U.S. military during the Cold War and FUD sites on the island remain point sources of POP contamination. We examined the effects of POP exposure on ninespine stickleback (Pungitius pungitius) collected from Troutman Lake in the village of Gambell as a model for human exposure and disease. During the Cold War, Troutman Lake was used as a dump site by the U.S. military. We found that PCB concentrations in stickleback exceeded the U.S. Environmental Protection Agency's guideline for unlimited consumption despite these fish being low trophic level organisms. We examined effects at three levels of biological organization: gene expression, endocrinology, and histomorphology. We found that ninespine stickleback from Troutman Lake exhibited suppressed gonadal development compared to threespine stickleback (Gasterosteus aculeatus) studied elsewhere. Troutman Lake stickleback also displayed two distinct hepatic phenotypes, one with lipid accumulation and one with glycogen-type vacuolation. We compared the transcriptomic profiles of these liver phenotypes using RNA sequencing and found significant upregulation of genes involved in ribosomal and metabolic pathways in the lipid accumulation group. Additionally, stickleback displaying liver lipid accumulation had significantly fewer thyroid follicles than the vacuolated phenotype. Our study and previous work highlight health concerns for people and wildlife due to pollution hotspots in the Arctic, and the need for health-protective remediation.

A novel method for extraction and quantification of feather triiodothyronine (T3) and application to ecotoxicology of Purple Martin (Progne subis).

Seventy-three percent of aerial insectivore species of birds breeding in North America have declined in the past five years. This decline is even greater in migratory insectivorous species, which face stressors in both their breeding and non-breeding ranges. The Purple Martin (Progne subis) is an aerial insectivore swallow that overwinters in South America and migrates to North America to breed. Purple Martin populations have declined by an estimated 25% since 1966. The eastern subspecies (P. subis subis) has declined the most and overwinters in the Amazon Basin, a region rich in environmental mercury (Hg) contamination. Previous studies reported elevated levels of Hg in feathers of this subspecies, which correlated negatively with body mass and fat reserves. Given the propensity of Hg to disrupt the endocrine system, and the role of thyroid hormones in regulating fat metabolism, this study quantifies concentrations of Hg and the thyroid hormone triiodothyronine (T3) in the feathers of P. subis subis. To our knowledge, this is the first study to extract and quantify T3 in feathers; thus, we developed, tested, and optimized a method for extracting T3 from feather tissue and validated an enzyme immunoassay (EIA) to quantify T3 in Purple Martin feathers. The developed method yielded acceptable results for both parallelism and accuracy. The observed T3 concentrations were statistically modeled along with total Hg (THg) concentrations, but these variables were not significantly correlated. This suggests that the observed variation in THg concentration may be insufficient to cause a discernible change in T3 concentration. Furthermore, the observed effect of breeding location on feather T3 concentration might have obscured any effect of Hg.

A novel method for extraction and quantification of feather triiodothyronine (T3) and application to ecotoxicology of Purple Martin (Progne subis)

Seventy-three percent of aerial insectivore species of birds breeding in North America have declined in the past five years. This decline is even greater in migratory insectivorous species, which face stressors in both their breeding and non-breeding ranges. The Purple Martin (Progne subis) is an aerial insectivore swallow that overwinters in South America and migrates to North America to breed. Purple Martin populations have declined by an estimated 25% since 1966. The eastern subspecies (P. subis subis) has declined the most and overwinters in the Amazon Basin, a region rich in environmental mercury (Hg) contamination. Previous studies reported elevated levels of Hg in feathers of this subspecies, which correlated negatively with body mass and fat reserves. Given the propensity of Hg to disrupt the endocrine system, and the role of thyroid hormones in regulating fat metabolism, this study quantifies concentrations of Hg and the thyroid hormone triiodothyronine (T3) in the feathers of P. subis subis. To our knowledge, this is the first study to extract and quantify T3 in feathers; thus, we developed, tested, and optimized a method for extracting T3 from feather tissue and validated an enzyme immunoassay (EIA) to quantify T3 in Purple Martin feathers. The developed method yielded acceptable results for both parallelism and accuracy. The observed T3 concentrations were statistically modeled along with total Hg (THg) concentrations, but these variables were not significantly correlated. This suggests that the observed variation in THg concentration may be insufficient to cause a discernible change in T3 concentration. Furthermore, the observed effect of breeding location on feather T3 concentration might have obscured any effect of Hg.

Interrelationships among feather mercury content, body condition and feather corticosterone in a Neotropical migratory bird, the Purple Martin (Progne subis subis).

Purple Martins (Progne subis) are migratory birds that breed in North America and overwinter and complete their molt in South America. Many of the breeding populations are declining. The eastern North American subspecies of Purple Martin (P. subis subis) comprises >90% of all Purple Martins. This subspecies overwinters and molts in the Amazon Basin, a region that is high in mercury (Hg) contamination, which raises the possibility that observed declines in Purple Martins could be linked to Hg exposure. Exposure to Hg results in numerous and systemic negative health outcomes, including endocrine disruption. Corticosterone (CORT) is a primary modulator of the stress and metabolic axes of vertebrates; thus, it is important in meeting metabolic and other challenges of migration. Because feathers accumulate Hg and hormones while growing, quantification of Hg and CORT in feathers provides an opportunity to retrospectively assess Hg exposure and adrenal activity of birds using minimally invasive methods. We evaluated interrelationships among concentrations of total Hg (THg) and CORT in feathers that grew in the Amazon Basin and body condition (mass, fat score) of these birds in North America. Concentrations of THg in Purple Martin feathers ranged from 1.103 to 8.740 µg/g dw, levels associated with negative physiological impacts in other avian species. Concentrations of CORT did not correlate with THg concentration at the time of feather growth. However, we found evidence that THg concentration may negatively impact the ability of Purple Martins to accumulate fat, which could impair migratory performance and survivorship due to the high energy requirements of migration. This finding suggests potential carryover effects of Hg contamination at the wintering grounds in the Amazon to the summer breeding grounds in North America.

Elevated mercury and PCB concentrations in Dolly Varden (Salvelinus malma) collected near a formerly used defense site on Sivuqaq, Alaska.

Environmental pollution causes adverse health effects in many organisms and contributes to health disparities for Arctic communities that depend on subsistence foods, including the Yupik residents of Sivuqaq (St. Lawrence Island), Alaska. Sivuqaq's proximity to Russia made it a strategic location for U.S. military defense sites during the Cold War. Two radar surveillance stations were installed on Sivuqaq, including at the Northeast Cape. High levels of persistent organic pollutants and toxic metals continue to leach from the Northeast Cape formerly used defense (FUD) site despite remediation efforts. We quantified total mercury (Hg) and polychlorinated biphenyl (PCB) concentrations, and carbon and nitrogen stable isotope signatures, in skin and muscle samples from Dolly Varden (Salvelinus malma), an important subsistence species. We found that Hg and PCB concentrations significantly differed across locations, with the highest concentrations found in fish collected near the FUD site. We found that 89% of fish collected from near the FUD site had Hg concentrations that exceeded the U.S. Environmental Protection Agency's (EPA) unlimited Hg-contaminated fish consumption screening level for subsistence fishers (0.049 µg/g). All fish sampled near the FUD site exceeded the EPA's PCB guidelines for cancer risk for unrestricted human consumption (0.0015 µg/g ww). Both Hg and PCB concentrations had a significant negative correlation with δ13C when sites receiving input from the FUD site were included in the analysis, but these relationships were insignificant when input sites were excluded. δ15N had a significant negative correlation with Hg concentration, but not with PCB concentration. These results suggest that the Northeast Cape FUD site remains a point source of Hg and PCB pollution and contributes to higher concentrations in resident fish, including subsistence species. Moreover, elevated Hg and PCB levels in fish near the FUD site may pose a health risk for Sivuqaq residents.

Case studies on longitudinal mercury content in humpback whale (Megaptera novaeangliae) baleen.

Quantification of contaminant concentrations in baleen whales is important for individual and population level health assessments but is difficult due to large migrations and infrequent resighings. The use of baleen allows for a multiyear retrospective analysis of contaminant concentrations without having to collect repeated samples from the same individual. Here we provide case studies of mercury analysis using cold vapor atomic absorption spectroscopy in three individual humpback whales (Megaptera novaeangliae), a 44.5-year-old female and two males aged ≥35 and 66 years, over approximately three years of baleen growth. Mercury concentrations in the female's baleen were consistently 2-3 times higher than in either male. Age did not affect mercury concentrations in baleen; the younger male had comparable levels to the older male. In the female, mercury concentrations in the baleen did not change markedly during pregnancy but mercury did spike during the first half of lactation. Stable isotope profiles suggest that diet likely drove the female's high mercury concentrations. In conclusion, variations in baleen mercury content can be highly individualistic. Future studies should compare sexes as well as different populations and species to determine how the concentrations of mercury and other contaminants vary by life history parameters and geography.

Interrelationships among feather mercury content, body condition and feather corticosterone in a Neotropical migratory bird, the Purple Martin (Progne subis subis)

Purple Martins (Progne subis) are migratory birds that breed in North America and overwinter and complete their molt in South America. Many of the breeding populations are declining. The eastern North American subspecies of Purple Martin (P. subis subis) comprises >90% of all Purple Martins. This subspecies overwinters and molts in the Amazon Basin, a region that is high in mercury (Hg) contamination, which raises the possibility that observed declines in Purple Martins could be linked to Hg exposure. Exposure to Hg results in numerous and systemic negative health outcomes, including endocrine disruption. Corticosterone (CORT) is a primary modulator of the stress and metabolic axes of vertebrates; thus, it is important in meeting metabolic and other challenges of migration. Because feathers accumulate Hg and hormones while growing, quantification of Hg and CORT in feathers provides an opportunity to retrospectively assess Hg exposure and adrenal activity of birds using minimally invasive methods. We evaluated interrelationships among concentrations of total Hg (THg) and CORT in feathers that grew in the Amazon Basin and body condition (mass, fat score) of these birds in North America. Concentrations of THg in Purple Martin feathers ranged from 1.103 to 8.740 μg/g dw, levels associated with negative physiological impacts in other avian species. Concentrations of CORT did not correlate with THg concentration at the time of feather growth. However, we found evidence that THg concentration may negatively impact the ability of Purple Martins to accumulate fat, which could impair migratory performance and survivorship due to the high energy requirements of migration. This finding suggests potential carryover effects of Hg contamination at the wintering grounds in the Amazon to the summer breeding grounds in North America.