Paralytic shellfish toxins in Alaskan Arctic food webs during the anomalously warm ocean conditions of 2019 and estimated toxin doses to Pacific walruses and bowhead whales.

Climate change-related ocean warming and reduction in Arctic sea ice extent, duration and thickness increase the risk of toxic blooms of the dinoflagellate Alexandrium catenella in the Alaskan Arctic. This algal species produces neurotoxins that impact marine wildlife health and cause the human illness known as paralytic shellfish poisoning (PSP). This study reports Paralytic Shellfish Toxin (PST) concentrations quantified in Arctic food web samples that include phytoplankton, zooplankton, benthic clams, benthic worms, and pelagic fish collected throughout summer 2019 during anomalously warm ocean conditions. PSTs (saxitoxin equivalents, STX eq.) were detected in all trophic levels with concentrations above the seafood safety regulatory limit (80 µg STX eq. 100 g-1) in benthic clams collected offshore on the continental shelf in the Beaufort, Chukchi, and Bering Seas. Most notably, toxic benthic clams (Macoma calcarea) were found north of Saint Lawrence Island where Pacific walruses (Odobenus rosmarus) are known to forage for a variety of benthic species, including Macoma. Additionally, fecal samples collected from 13 walruses harvested for subsistence purposes near Saint Lawrence Island during March to May 2019, all contained detectable levels of STX, with fecal samples from two animals (78 and 72 µg STX eq. 100 g-1) near the seafood safety regulatory limit. In contrast, 64% of fecal samples from zooplankton-feeding bowhead whales (n = 9) harvested between March and September 2019 in coastal waters of the Beaufort Sea near Utqiagvik (formerly Barrow) and Kaktovik were toxin-positive, and those levels were significantly lower than in walruses (max bowhead 8.5 µg STX eq. 100 g-1). This was consistent with the lower concentrations of PSTs found in regional zooplankton prey. Maximum ecologically-relevant daily toxin doses to walruses feeding on clams and bowhead whales feeding on zooplankton were estimated to be 21.5 and 0.7 µg STX eq. kg body weight-1 day-1, respectively, suggesting that walruses had higher PST exposures than bowhead whales. Average and maximum STX doses in walruses were in the range reported previously to cause illness and/or death in humans and humpback whales, while bowhead whale doses were well below those levels. These findings raise concerns regarding potential increases in PST/STX exposure risks and health impacts to Arctic marine mammals as ocean warming and sea ice reduction continue.

Ice seals as sentinels for algal toxin presence in the Pacific Arctic and subarctic marine ecosystems.

Domoic acid (DA) and saxitoxin (STX)-producing algae are present in Alaskan seas, presenting exposure risks to marine mammals that may be increasing due to climate change. To investigate potential increases in exposure risks to four pagophilic ice seal species (Erignathus barbatus, bearded seals; Pusa hispida, ringed seals; Phoca largha, spotted seals; and Histriophoca fasciata, ribbon seals), this study analyzed samples from 998 seals harvested for subsistence purposes in western and northern Alaska during 2005-2019 for DA and STX. Both toxins were detected in bearded, ringed, and spotted seals, though no clinical signs of acute neurotoxicity were reported in harvested seals. Bearded seals had the highest prevalence of each toxin, followed by ringed seals. Bearded seal stomach content samples from the Bering Sea showed a significant increase in DA prevalence with time (logistic regression, p = .004). These findings are consistent with predicted northward expansion of DA-producing algae. A comparison of paired samples taken from the stomachs and colons of 15 seals found that colon content consistently had higher concentrations of both toxins. Collectively, these results suggest that ice seals, particularly bearded seals (benthic foraging specialists), are suitable sentinels for monitoring HAB prevalence in the Pacific Arctic and subarctic.

Polycyclic aromatic hydrocarbons and risk to threatened and endangered Chinook salmon in the Lower Columbia River estuary.

Polycyclic aromatic hydrocarbons (PAHs), derived from oil and fuel combustion, are ubiquitous nonpoint source pollutants that can have a number of detrimental effects on fish and wildlife. In this study, we monitored PAH exposure in outmigrant juvenile Chinook salmon from the Lower Columbia River to evaluate the risk that these contaminants might pose to the health and recovery of threatened and endangered salmonids. Juvenile Chinook salmon (Oncorhynchus tshawytscha) were collected by beach seine from five sites in the Lower Columbia River from Bonneville Dam to the mouth of the estuary (Warrendale, the Willamette-Columbia Confluence, Columbia City, Beaver Army Terminal, and Point Adams) and from a site in the Lower Willamette near downtown Portland (Morrison Street Bridge). Sediment samples were also collected at the same sites. Concentrations of PAHs in sediment samples were relatively low at all sites with average total PAH concentrations <1000 ng/g dry weight (wt.). However, we found PAHs in stomach contents of salmon from all sites at concentrations ranging from <100 to >10,000 ng/g wet wt. Metabolites of low and high molecular-weight PAHs were also detected in bile of salmon from all sites; for metabolites fluorescing at phenanthrene (PHN) wavelengths, concentrations ranged from 1.1 to 6.0 µg/mg bile protein. Levels of PAHs in stomach contents and PAH metabolites in bile were highest in salmon from the Morrison Street Bridge site in Portland and the Willamette-Columbia Confluence, Columbia City, and Beaver Army Terminal sites. Mean PAH concentrations measured in some stomach content samples from the Columbia City, Beaver Army Terminal, and Morrison Street Bridge sites were near the threshold concentration (approximately 7200-7600 ng/g wet wt.) associated with variability and immune dysfunction in juvenile salmonids (Meador et al., Can J Fish Aquat Sci 63:2364-2376, 2006; Bravo et al., Environ Toxicol Chem 30:704-714, 2011). Mean levels of biliary fluorescent aromatic compounds (FACs)-PHN in juvenile Chinook collected at the Morrison Street Bridge site in Portland, at the Confluence and Columbia City sites, and at the Beaver Army Terminal site were at or above a threshold effect concentration of 2 µg/mg protein for FACs-PHN linked to growth impairment, altered energetics, and reproductive effects (Meador et al., Environ Toxicol Chem 27(4):845-853, 2008). These findings suggest that PAHs in the food chain are a potential source of injury to juvenile salmon in the Lower Columbia and Lower Willamette rivers.

Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish.

Exposure to high concentrations of crude oil produces a lethal syndrome of heart failure in fish embryos. Mortality is caused by cardiotoxic polycyclic aromatic hydrocarbons (PAHs), ubiquitous components of petroleum. Here, we show that transient embryonic exposure to very low concentrations of oil causes toxicity that is sublethal, delayed, and not counteracted by the protective effects of cytochrome P450 induction. Nearly a year after embryonic oil exposure, adult zebrafish showed subtle changes in heart shape and a significant reduction in swimming performance, indicative of reduced cardiac output. These delayed physiological impacts on cardiovascular performance at later life stages provide a potential mechanism linking reduced individual survival to population-level ecosystem responses of fish species to chronic, low-level oil pollution.