Using Domestic and Free-Ranging Arctic Canid Models for Environmental Molecular Toxicology Research.

The use of sentinel species for population and ecosystem health assessments has been advocated as part of a One Health perspective. The Arctic is experiencing rapid change, including climate and environmental shifts, as well as increased resource development, which will alter exposure of biota to environmental agents of disease. Arctic canid species have wide geographic ranges and feeding ecologies and are often exposed to high concentrations of both terrestrial and marine-based contaminants. The domestic dog (Canis lupus familiaris) has been used in biomedical research for a number of years and has been advocated as a sentinel for human health due to its proximity to humans and, in some instances, similar diet. Exploiting the potential of molecular tools for describing the toxicogenomics of Arctic canids is critical for their development as biomedical models as well as environmental sentinels. Here, we present three approaches analyzing toxicogenomics of Arctic contaminants in both domestic and free-ranging canids (Arctic fox, Vulpes lagopus). We describe a number of confounding variables that must be addressed when conducting toxicogenomics studies in canid and other mammalian models. The ability for canids to act as models for Arctic molecular toxicology research is unique and significant for advancing our understanding and expanding the tool box for assessing the changing landscape of environmental agents of disease in the Arctic.

A study on the genetic population structure and the tetrodotoxin content of rough-skinned newts, Taricha granulosa (Salamandridae), from their northern range of distribution.

Rough-skinned newts, Taricha granulosa, which contain tetrodotoxin (TTX), a potent neurotoxin, are widely distributed along the west-coast of North America up to British Columbia (BC), Canada, and Southeast Alaska. Their genetic population structure using DNA-microsatellites and the TTX-content of specimens from British Columbia (Prince Rupert area) and Alaska (Revillagigedo Island, Shelter Island, and Juneau) were analysed. TTX-concentrations were low in newts from BC and Revillagigedo Island, but high in specimens from mainland Juneau, which had been deliberately introduced from Shelter Island, where TTX was not detectable in the individuals sampled. No significant genetic differences were detected between these populations, which may correlate with the high intraspecies variability of TTX. It is still an open question, which factors favour or induce the toxin production in the newts.

Paralytic shellfish toxins associated with Arctic Tern mortalities in Alaska.

Harmful algal blooms produce biotoxins that can injure or kill fish, wildlife, and humans. These blooms occur naturally but have intensified in many locations globally due to recent climatic changes, including ocean warming. Such changes are especially pronounced in northern regions, where the effects of paralytic shellfish toxins (PSTs) on marine wildlife are of growing concern. In Alaska, seabird mortality events have increased in frequency, magnitude, and duration since 2015 alongside anomalously high ocean temperatures. Although starvation has been implicated as the apparent cause of death in many of these die-offs, saxitoxin (STX) and other PSTs have been identified as possible contributing factors. Here, we describe a mortality event at a nesting colony of Arctic Terns (Sterna paradisaea) near Juneau, Alaska in 2019 and report elevated concentrations of PSTs in bird, forage fish, and mussel samples. Concentrations of STX and other PSTs in tern tissues (2.5-51.2 µg 100g-1 STX-equivalents [STX-eq]) were of similar magnitude to those reported from other PST-induced bird die-offs. We documented high PST concentrations in blue mussels (>11,000 µg 100g-1 STX-eq; Mytilus edulis spp.) collected from nearby beaches, as well as in forage fish (up to 494 µg 100g-1 STX-eq) retrieved from Arctic Tern nests, thereby providing direct evidence of PST exposure via the terns' prey. At maximum concentrations measured in this study, a single 5 g Pacific Sand Lance (Ammodytes personatus) could exceed the median lethal STX dose (LD50) currently estimated for birds, offering strong support for PSTs as a likely source of tern mortality. In addition to describing this localized bird mortality event, we used existing energetics data from adult and nestling Arctic Terns to calculate estimated cumulative daily PST exposure based on ecologically relevant concentrations in forage fish. Our estimates revealed potentially lethal levels of PST exposure even at relatively low (≤30 ug 100g-1 STX-eq) toxin concentrations in prey. These findings suggest that PSTs present a significant hazard to Arctic Terns and other northern seabirds and should be included in future investigations of avian mortality events as well as assessments of population health.

Random forest classification to determine environmental drivers and forecast paralytic shellfish toxins in Southeast Alaska with high temporal resolution.

Paralytic shellfish poison toxins (PSTs) produced by the dinoflagellate in the genus Alexandrium are a threat to human health and subsistence lifestyles in Southeast Alaska. It is important to understand the drivers of Alexandrium blooms to inform shellfish management and aquaculture, as well as to predict trends of PST in a changing climate. In this study, we aggregate environmental data sets from multiple agencies and tribal partners to model and predict concentrations of PSTs in Southeast Alaska from 2016 to 2019. We used daily PST concentrations interpolated from regularly sampled blue mussels (Mytilus trossulus) analyzed for total PSTs using a receptor binding assay. We then created random forest models to classify shellfish above and below a threshold of toxicity (80 µg 100 g-1) and used two methods to determine variable importance. We obtained a multivariate model with key variables being sea surface temperature, salinity, freshwater discharge, and air temperature. We then used a similar model trained using lagged environmental variables to hindcast out-of-sample (OOS) shellfish toxicities during April-October in 2017, 2018, and 2019. Hindcast OOS accuracies were low (37-50%); however, we found forecasting using environmental variables may be useful in predicting the timing of early summer blooms. This study reinforces the efficacy of machine learning to determine important drivers of harmful algal blooms, although more complex models incorporating other parameters such as toxicokinetics are likely needed for accurate regional forecasts.

The Southeast Alaska Tribal Ocean Research (SEATOR) Partnership: Addressing Data Gaps in Harmful Algal Bloom Monitoring and Shellfish Safety in Southeast Alaska.

Many communities in Southeast Alaska harvest shellfish such as mussels and clams as an important part of a subsistence or traditional diet. Harmful algal blooms (HABs) of phytoplankton such as Alexandrium spp. produce toxins that can accumulate in shellfish tissues to concentrations that can pose a hazard for human health. Since 2013, several tribal governments and communities have pooled resources to form the Southeast Alaska Tribal Ocean Research (SEATOR) network, with the goal of minimizing risks to seafood harvest and enhancing food security. SEATOR monitors toxin concentrations in shellfish and collects and consolidates data on environmental variables that may be important predictors of toxin levels such as sea surface temperature and salinity. Data from SEATOR are publicly available and are encouraged to be used for the development and testing of predictive algorithms that could improve seafood risk assessment in Southeast Alaska. To date, more than 1700 shellfish samples have been analyzed for paralytic shellfish toxins (PSTs) in more than 20 locations, with potentially lethal concentrations observed in blue mussels (Mytilus trossulus) and butter clams (Saxidomus gigantea). Concentrations of PSTs exhibit seasonality in some species, and observations of Alexandrium are correlated to sea surface temperature and salinity; however, concentrations above the threshold of concern have been found in all months, and substantial variation in concentrations of PSTs remain unexplained.

Concentrations of organohalogens (PCBs, DDTs, PBDEs) in hunted and stranded Northern sea otters (Enhydra lutris kenyoni) in Alaska from 1992 to 2010: Links to pathology and feeding ecology.

Many organohalogen compounds (OHCs) are persistent organic pollutants (POPs) found in appreciable concentrations in marine predators. While production of some POPs has declined or ceased in recent decades, their capacity for global transport and bioaccumulation results in observations of unchanging or increasing concentrations in marine systems. Sea otters (Enhydra lutris) have been advocated as an environmental sentinel for contaminants due to their longevity, site fidelity and prey species that often overlap with human consumption. Using archived (1992-2010) samples of livers from Northern sea otters (n = 50) from Alaska we examine concentrations of chlordanes (CHLs), polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDTs), and polybrominated diphenyl ethers (PBDEs) and associated metabolites. We found some evidence for declining ΣPCBs over the two decades, however for most animals concentrations were low compared to toxicological thresholds. Six animals had relatively high concentrations of ΣPCBs (mean = 262,000 ng/g lipid weight), ΣDDTs (mean = 8,800 ng/g lw), and ΣPBDEs (mean = 4,600 ng/g lw), with four of these six animals experiencing hepatic parasitism or hepatitis. In order to assess whether differences in POP concentrations are associated with feeding ecology, we examined stable isotopes of C and N in archived muscle and whisker samples. In general, there were no significant relationships between ΣPOP concentrations and stable isotope ratios. There were small differences in stable isotope profiles in animals with high POP concentrations, although it was unclear if these differences were due to feeding ecology or disease processes. This study highlights the importance of considering feeding ecology and necropsy (health and disease status) data while conducting contaminant surveys, and confirms some previous reports of trends in OHCs in Alaska marine mammals.

Variation in bioaccumulation of persistent organic pollutants based on octanol-air partitioning: Influence of respiratory elimination in marine species.

Risk assessments of persistent organic pollutants (POPs) are often based on octanol-water (KOW) partitioning dynamics and may not adequately reflect bioaccumulation in air-breathing organisms. It has been suggested that compounds with low KOW and high octanol-air partitioning (KOA) coefficients have the potential to bioaccumulate in air-breathing organisms, including marine mammals. Here we evaluate differences in concentrations of POPs for two trophically matched Arctic species, spotted seal (Phoca largha) and sheefish (Stenodus leucichthys). We compared concentrations of 108 POPs in matched tissues (liver and muscle) across three ranges of KOW. We found a significant positive correlation between POP concentration and log KOA in spotted seal tissues for low log KOW compounds (log KOW <5.5, p<0.05). This provides further evidence for empirical models and observed bioaccumulation patterns in air-breathing organisms, and highlights the potential for bioaccumulation of these compounds in Arctic marine mammals.