Sentinel California sea lions provide insight into legacy organochlorine exposure trends and their association with cancer and infectious disease.

BackgroundOrganochlorine contaminants (OCs), like polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethanes (DDTs), are widespread marine pollutants resulting from massive historical use and environmental persistence. Exposure to and health effects of these OCs in the marine environment may be examined by studying California sea lions (Zalophus californianus), which are long lived, apex predators capable of accumulating OCs.MethodsWe evaluated PCB and DDT levels in 310 sea lions sampled between 1992 and 2007: 204 individuals stranded along the coast of central California, 60 healthy males from Washington State, and 46 healthy females from southern California. Lipid-normalized contaminant concentrations were analyzed using general linear models and logistic regression to ascertain temporal trends; differences between stranded and healthy sea lions; and association of organochlorines with sex, age, and presence of cancer or fatal infectious disease.ResultsConcentrations of the contaminants in stranded adults decreased over time in the study period (adjusted for sex, as adult males had higher mean blubber concentrations than adult females and juveniles). Cancer was almost eight and six times more likely in animals with higher summed PCBs and DDTs, compared to those with lower levels (95% CI 5.55-10.51 and 4.54-7.99, respectively). Fatal infectious diseases were similarly seven and five times more likely in animals with higher contaminant burdens (95% CI 4.20-10.89 and 3.27-7.86, respectively). Mean contaminant loads were significantly higher in stranded sea lions than in healthy live captured animals (p < 0.001).ConclusionOrganochlorine contamination has significant associations with health outcomes in California sea lions, raising concerns for humans and other animals eating tainted seafood. While environmental exposure to these organochlorines appears to be decreasing over time based on levels in sea lion tissues, their persistence in the environment and food web for all predators, including humans, and the associated serious health risks, warrant monitoring, possibly through sentinel species like marine mammals

Sentinel California sea lions provide insight into legacy organochlorine exposure trends and their association with cancer and infectious disease

Background: Organochlorine contaminants (OCs), like polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethanes (DDTs), are widespread marine pollutants resulting from massive historical use and environmental persistence. Exposure to and health effects of these OCs in the marine environment may be examined by studying California sea lions (Zalophus californianus), which are long lived, apex predators capable of accumulating OCs. Methods: We evaluated PCB and DDT levels in 310 sea lions sampled between 1992 and 2007: 204 individuals stranded along the coast of central California, 60 healthy males from Washington State, and 46 healthy females from southern California. Lipid-normalized contaminant concentrations were analyzed using general linear models and logistic regression to ascertain temporal trends; differences between stranded and healthy sea lions; and association of organochlorines with sex, age, and presence of cancer or fatal infectious disease. Results: Concentrations of the contaminants in stranded adults decreased over time in the study period (adjusted for sex, as adult males had higher mean blubber concentrations than adult females and juveniles). Cancer was almost eight and six times more likely in animals with higher summed PCBs and DDTs, compared to those with lower levels (95% CI 5.55-10.51 and 4.54-7.99, respectively). Fatal infectious diseases were similarly seven and five times more likely in animals with higher contaminant burdens (95% CI 4.20-10.89 and 3.27-7.86, respectively). Mean contaminant loads were significantly higher in stranded sea lions than in healthy live captured animals (p b 0.001). Conclusion: Organochlorine contamination has significant associations with health outcomes in California sea lions, raising concerns for humans and other animals eating tainted seafood. While environmental exposure to these organochlorines appears to be decreasing over time based on levels in sea lion tissues, their persistence in the environment and food web for all predators, including humans, and the associated serious health risks, warrant monitoring, possibly through sentinel species like marine mammals

Highly contaminated river otters (Lontra canadensis) are effective biomonitors of environmental pollutant exposure

River otters (Lontra canadensis) are apex predators that bioaccumulate contaminants via their diet, potentially serving as biomonitors of watershed health. They reside throughout the Green-Duwamish River, WA (USA), a watershed encompassing an extreme urbanization gradient, including a US Superfund site slated for a 17-year remediation. The objectives of this study were to document baseline contaminant levels in river otters, assess otters’ utility as top trophic-level biomonitors of contaminant exposure, and evaluate the potential for health impacts on this species. We measured a suite of contaminants of concern, lipid content, nitrogen stable isotopes (δ15N), and microsatellite DNA markers in 69 otter scat samples collected from twelve sites. Landcover characteristics were used to group sampling sites into industrial (Superfund site), suburban, and rural development zones. Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ether flame-retardants (PBDEs), dichlorodiphenyl-trichloroethane and its metabolites (DDTs), and polycyclic aromatic hydrocarbons (PAHs) increased significantly with increasing urbanization, and were best predicted by models that included development zone, suggesting that river otters are effective biomonitors, as defined in this study. Diet also played an important role, with lipid content, δ15N or both included in all best models. We recommend river otter scat be included in evaluating restoration efforts in this Superfund site, and as a potentially useful monitoring tool wherever otters are found. We also report ΣPCB and ΣPAH exposures among the highest published for wild river otters, with almost 70% of samples in the Superfund site exceeding established levels of concern.publishedVersio

Assessing the threat of toxic contaminants to early marine survival of Chinook salmon in the Salish Sea

Human development of the Salish Sea has resulted in loss and modification of salmonid habitats, including reduced habitat quality due to contaminant inputs, particularly in the lower reaches of rivers and estuaries of the central Puget Sound. Chemical contaminants released into the Salish Sea from anthropogenic sources can reduce the health and productivity of salmon. Juvenile salmon are exposed to contaminants in freshwater, estuarine, and marine habitats but they are particularly vulnernable as they transition from fresh to saltwater because this life history stage is especially sensitive to stressors that may reduce their early marine survival. Reduced growth and disease resistance have been demonstrated for juvenile Chinook salmon exposed to environmentally relevant contaminant levels; however, synoptic, Puget Sound-wide surveys to assess the extent and magnitude of contaminant exposure are lacking. In this study we measured exposure of juvenile Chinook salmon to chemicals of concern that enter Puget Sound via stormwater, wastewater treatment facilities, atmospheric deposition to marine waters, and groundwater. During the spring and summer of 2013, outmigrating fish were sampled from the river mouthes and two adjacent marine shorelines at each of five Puget Sound river-estuary systems: Skagit, Snohomish, Green/Duwamish, Puyallup/Hylebos, and Nisqually. We (1) report the extent and magnitude of exposure, (2) compare exposure in outmigrants across five major river-estuary systems, and (3) evaluate potential effects on marine survival. Results will be used to establish a time series of contaminant conditions in juvenile Chinook salmon to measure the effectiveness of current toxics reductions strategies and actions, inform future pollution reduction efforts, and enhanced recovery of Chinook salmon

Persistent contaminants and herpesvirus OtHV1 are positively associated with cancer in wild California Sea Lions (Zalophus californianus)

This work was funded by the Geoffrey Hughes Fellowship, the National Institutes of Health (Fogarty International Center) and National Science Foundation joint program for the Ecology of Infectious Disease, the National Marine Fisheries Service Marine Mammal Heath and Stranding Program, and the Natural Environment Research Council grant number NE/R015007/.The prevalence of cancer in wild California sea lions (Zalophus californianus) is one of the highest amongst mammals, with 18–23% of adult animals examined post-mortem over the past 40 years having urogenital carcinoma. To date, organochlorines, genotype and infection with Otarine herpesvirus-1 (OtHV-1) have been identified in separate studies using distinct animals as associated with this carcinoma. Multi-year studies using large sample sizes to investigate the relative importance of multiple factors on marine mammal health are rare due to logistical and ethical challenges. The objective of this study was to use a case control approach with samples from 394 animals collected over 20 years in a multifactorial analysis to explore the relative importance of distinct factors identified to date as associated with sea lion cancer in the likelihood of sea lion carcinoma. Stepwise regression indicated that the best model to explain carcinoma occurrence included herpesvirus status, contaminant exposure, and blubber depth, but not genotype at a single microsatellite locus, PV11. The odds of carcinoma was 43.57 times higher in sea lions infected with OtHV-1 (95% CI 14.61, 129.96, p <0.001), and 1.48 times higher for every unit increase in the loge[contaminant concentrations], ng g–1 (an approximate tripling of concentration), in their blubber (95% CI 1.11, 1.97, p <0.007), after controlling for the effect of blubber depth. These findings demonstrate the importance of contaminant exposure combined with OtHV1 infection, in the potential for cancer occurrence in wild sea lions.Publisher PDFPeer reviewe

Effects of polycyclic aromatic hydrocarbons (PAHs) on Pacific herring (Clupea pallasii) embryos exposed to creosote-treated pilings related to a piling removal project in Quilcene Bay, Washington

Fish embryos spawned in Puget Sound nearshore marine habitats face a risk of exposure to a wide variety of toxic chemical pollutants during their incubation. Of particular concern are polycyclic aromatic hydrocarbons (PAHs), chemicals originating from oil spills, combusted fossil fuels, and creosote-treated pilings (CTPs). Removal of CTPs and prohibiting their use in marine waters are two recovery practices aimed at reducing PAHs and other creosote-related chemicals in marine waters. We used manually spawned and field-deployed Pacific herring embryos as a sensitive indicator of PAH exposure from CTPs, to test the efficacy of a CTP removal project in Quilcene Bay Washington. Embryos were deployed near CTPs in a 100-year-old derelict CTP field (1) before the CTPs were removed, (2) just after the removal process, to evaluate whether PAHs were released during removal, and (3) one year later, to evaluate whether PAHs lingered after CTP removal. Embryos incubated in the undisturbed CTP field prior to CTP removal exhibited PAH body burdens approximately five times higher than at reference areas, though total PAHs in the CTP-field embryos were below health effects thresholds. The CTP removal project was not fully completed during this study; CTP debris remained in the piling field and many CTPs were cut at the seafloor, resulting in freshly exposed CTP surfaces after the removal project ended. PAH concentrations in embryos sampled during and after CTP removal were 25x to 83x higher than reference embryos, and many exceeded health effects thresholds. PAH concentrations in embryos after CTP removal correlated with distance from former CTP locations. In addition, expression of cyp1a, a gene involved in PAH-detoxification, was correlated with PAH body burden. These results link embryo health with toxic contaminants associated with CTPs and illustrate the importance of fastidious adherence to appropriate CTP removal protocols to avoid contaminant risks to biota

Recurrent Die-Offs of Adult Coho Salmon Returning to Spawn in Puget Sound Lowland Urban Streams

Several Seattle-area streams in Puget Sound were the focus of habitat restoration projects in the 1990s. Post-project effectiveness monitoring surveys revealed anomalous behaviors among adult coho salmon returning to spawn in restored reaches. These included erratic surface swimming, gaping, fin splaying, and loss of orientation and equilibrium. Affected fish died within hours, and female carcasses generally showed high rates (>90%) of egg retention. Beginning in the fall of 2002, systematic spawner surveys were conducted to 1) assess the severity of the adult die-offs, 2) compare spawner mortality in urban vs. non-urban streams, and 3) identify water quality and spawner condition factors that might be associated with the recurrent fish kills. The forensic investigation focused on conventional water quality parameters (e.g., dissolved oxygen, temperature, ammonia), fish condition, pathogen exposure and disease status, and exposures to metals, polycyclic aromatic hydrocarbons, and current use pesticides. Daily surveys of a representative urban stream (Longfellow Creek) from 2002–2009 revealed premature spawner mortality rates that ranged from 60–100% of each fall run. The comparable rate in a non-urban stream was <1% (Fortson Creek, surveyed in 2002). Conventional water quality, pesticide exposure, disease, and spawner condition showed no relationship to the syndrome. Coho salmon did show evidence of exposure to metals and petroleum hydrocarbons, both of which commonly originate from motor vehicles in urban landscapes. The weight of evidence suggests that freshwater-transitional coho are particularly vulnerable to an as-yet unidentified toxic contaminant (or contaminant mixture) in urban runoff. Stormwater may therefore place important constraints on efforts to conserve and recover coho populations in urban and urbanizing watersheds throughout the western United States

Predicting the effects of polychlorinated biphenyls on cetacean populations through impacts on immunity and calf survival

This work was supported by funding from the International Whaling Commission's Pollution 2000+Program, the U.S. NOAA/NFMS Health and Stranding Response Program and the UK's Natural Environment Research Council (Grant Code SMRU 10001).The potential impact of exposure to polychlorinated biphenyls (PCBs) on the health and survival of cetaceans continues to be an issue for conservation and management, yet few quantitative approaches for estimating population level effects have been developed. An individual based model (IBM) for assessing effects on both calf survival and immunity was developed and tested. Three case study species (bottlenose dolphin, humpback whale and killer whale) in four populations were taken as examples and the impact of varying levels of PCB uptake on achievable population growth was assessed. The unique aspect of the model is its ability to evaluate likely effects of immunosuppression in addition to calf survival, enabling consequences of PCB exposure on immune function on all age-classes to be explored. By incorporating quantitative tissue concentration-response functions from laboratory animal model species into an IBM framework, population trajectories were generated. Model outputs included estimated concentrations of PCBs in the blubber of females by age, which were then compared to published empirical data. Achievable population growth rates were more affected by the inclusion of effects of PCBs on immunity than on calf survival, but the magnitude depended on the virulence of any subsequent encounter with a pathogen and the proportion of the population exposed. Since the starting population parameters were from historic studies, which may already be impacted by PCBs, the results should be interpreted on a relative rather than an absolute basis. The framework will assist in providing quantitative risk assessments for populations of concern.PostprintPostprintPeer reviewe