Significance: The neurotoxin-producing dinoflagellate Alexandrium catenella is shown to be distributed widely and at high concentrations in bottom sediments and surface waters of the Alaskan Arctic. Future blooms are likely to be large and frequent given hydrographic and bathymetric features that support high cell and cyst accumulations, and warming temperatures that promote bloom initiation from cysts in bottom sediments and cell division in surface waters. As the region undergoes an unprecedented regime shift, the exceptionally widespread and dense cyst and cell distributions represent a significant threat to Arctic communities that are heavily dependent upon subsistence harvesting of marine resources. These observations also highlight how warming can facilitate range expansions of harmful algal bloom species into waters where temperatures were formerly unfavorable.
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 Utqiaġvik (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.
10 July 2024 in Limnology and Oceanography Letters
In recent years, blooms of the neurotoxic dinoflagellate Alexandrium catenella have been documented in Pacific Arctic waters, and the paralytic shellfish toxins (PSTs) that this species produces have been detected throughout the food web. These observations have raised significant concerns about the role that harmful algal blooms (HABs) will play in a rapidly changing Arctic. During a research cruise in summer 2022, a massive bloom of A. catenella was detected in real time as it was advected through the Bering Strait region. The bloom was exceptional in both spatial scale and density, extending > 600 km latitudinally, reaching concentrations > 174,000 cells L−1, and producing high‐potency PST congeners. Throughout the event, coastal stakeholders in the region were engaged and a multi‐faceted community response was mobilized. This unprecedented bloom highlighted the urgent need for response capabilities to ensure safe utilization of critical marine resources in a region that has little experience with HABs.
Over the last two decades, ocean warming and rapid loss of sea ice have dramatically changed the Pacific Arctic marine environment1–3. These changes are predicted to increase harmful algal bloom prevalence and toxicity, as rising temperatures and larger open water areas are more favourable for growth of some toxic algal species4. It is well known that algal toxins are transferred through food webs during blooms and can have negative impacts on wildlife and human health5–7. Yet, there are no long-term quantitative reports on algal toxin presence in Arctic food webs to evaluate increasing exposure risks. In the present study, algal toxins were quantified in bowel samples collected from 205 bowhead whales harvested for subsistence purposes over 19 years. These filter-feeding whales served as integrated food web samplers for algal toxin presence in the Beaufort Sea as it relates to changing environmental conditions over two decades. Algal toxin prevalences and concentrations were significantly correlated with ocean heat flux, open water area, wind velocity and atmospheric pressure. These results provide confirmative oceanic, atmospheric and biological evidence for increasing algal toxin concentrations in Arctic food webs due to warming ocean conditions. This approach elucidates breakthrough mechanistic connections between warming oceans and increasing algal toxin exposure risks to Arctic wildlife, which threatens food security for Native Alaskan communities that have been reliant on marine resources for subsistence for 5,000 years (ref. 8).
In August 2024, a northern fur seal mortality event was observed on St. Paul Island, AK in the southeast (SE) Bering Sea. Ten seals in good body condition were found dead along with large accumulations of dead fish on Benson Beach located on St. Paul Island. Full necropsies of the five available adult seals, one pup, and several fish did not reveal any overt causes of death. Testing of tissues for the algal neurotoxins domoic acid (DA) and saxitoxin (STX) confirmed the presence of STX in multiple tissues and physiological exposure in all five adult NFS and the two fish available for testing. DA was not detected in any samples. Complimentary samples of the SE Bering Sea ecosystem during the same time frame and location as the die off revealed bloom densities of Alexandrium catenella (the dinoflagellate that produces STX), large A. catenella cyst beds, and high prevalences of STX in fish (100%, n = 22), zooplankton (93%, n = 28), clams (100%, n = 10) and worms (93% n = 15) in the foraging area of NFS. High STX concentrations were observed in fish, clams, worms, and NFS urine, providing compelling evidence for a STX poisoning event.
Clams are efficient vectors of potent algal neurotoxins, a suite of saxitoxin (STX) congeners collectively called paralytic shellfish toxins (PSTs), to higher trophic levels. The Alaskan Arctic is a region facing an expanding threat from PSTs due to ocean warming, yet little is known about PSTs in clams from this region. Quantifying total toxicity in bivalves requires analytical techniques, such as high-performance liquid chromatography (HPLC). Enzyme-linked immunosorbent assays (ELISAs) are an efficient but only semi-quantitative method for measuring clam toxicity. PSTs (STX eq.) were measured in split clam samples (n = 16) from the Alaskan Arctic using ELISA and HPLC methods to develop a preliminary linear model for conservatively estimating total toxicity in clams from ELISA toxin values (R2adj = 0.95, p < 0.001). Profiles of PST congeners and total toxicity using HPLC were also assessed in additional clams (n = 36 additional, n = 52 total). Clams contained mostly potent PST congeners, and over half of the clams had PST concentrations above the seafood regulatory limit. These data will help assess the exposure risks of PSTs in Arctic marine food webs, as harmful algal bloom activity is predicted to increase as the Arctic continues to warm.