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.

Return of warm conditions in the southeastern Bering Sea: Phytoplankton - Fish.

In 2014, the Bering Sea shifted back to warmer ocean temperatures (+2 oC above average), bringing concern for the potential for a new warm stanza and broad biological and ecological cascading effects. In 2015 and 2016 dedicated surveys were executed to study the progression of ocean heating and ecosystem response. We describe ecosystem response to multiple, consecutive years of ocean warming and offer perspective on the broader impacts. Ecosystem changes observed include reduced spring phytoplankton biomass over the southeast Bering Sea shelf relative to the north, lower abundances of large-bodied crustacean zooplankton taxa, and degraded feeding and body condition of age-0 walleye pollock. This suggests poor ecosystem conditions for young pollock production and the risk of significant decline in the number of pollock available to the pollock fishery in 2-3 years. However, we also noted that high quality prey, large copepods and euphausiids, and lower temperatures in the north may have provided a refuge from poor conditions over the southern shelf, potentially buffering the impact of a sequential-year warm stanza on the Bering Sea pollock population. We offer the hypothesis that juvenile (age-0, age-1) pollock may buffer deleterious warm stanza effects by either utilizing high productivity waters associated with the strong, northerly Cold Pool, as a refuge from the warm, low production areas of the southern shelf, or by exploiting alternative prey over the southern shelf. We show that in 2015, the ocean waters influenced by spring sea ice (the Cold Pool) supported robust phytoplankton biomass (spring) comprised of centric diatom chains, a crustacean copepod community comprised of large-bodied taxa (spring, summer), and a large aggregation of midwater fishes, potentially young pollock. In this manner, the Cold Pool may have acted as a trophic refuge in that year. The few age-0 pollock occurring over the southeast shelf consumed high numbers of euphausiids which may have provided a high quality alternate prey. In 2016 a retracted Cold Pool precluded significant refuging in the north, though pollock foraging on available euphausiids over the southern shelf may have mitigated the effect of warm waters and reduced large availability of large copepods. This work presents the hypothesis that, in the short term, juvenile pollock can mitigate the drastic impacts of sustained warming. This short-term buffering, combined with recent observations (2017) of renewed sea ice presence over southeast Bering Sea shelf and a potential return to average or at least cooler ecosystem conditions, suggests that recent warm year stanza (2014-2016) effects to the pollock population and fishery may be mitigated.

Spatial match-mismatch between juvenile fish and prey provides a mechanism for recruitment variability across contrasting climate conditions in the eastern Bering Sea.

Understanding mechanisms behind variability in early life survival of marine fishes through modeling efforts can improve predictive capabilities for recruitment success under changing climate conditions. Walleye pollock (Theragra chalcogramma) support the largest single-species commercial fishery in the United States and represent an ecologically important component of the Bering Sea ecosystem. Variability in walleye pollock growth and survival is structured in part by climate-driven bottom-up control of zooplankton composition. We used two modeling approaches, informed by observations, to understand the roles of prey quality, prey composition, and water temperature on juvenile walleye pollock growth: (1) a bioenergetics model that included local predator and prey energy densities, and (2) an individual-based model that included a mechanistic feeding component dependent on larval development and behavior, local prey densities and size, and physical oceanographic conditions. Prey composition in late-summer shifted from predominantly smaller copepod species in the warmer 2005 season to larger species in the cooler 2010 season, reflecting differences in zooplankton composition between years. In 2010, the main prey of juvenile walleye pollock were more abundant, had greater biomass, and higher mean energy density, resulting in better growth conditions. Moreover, spatial patterns in prey composition and water temperature lead to areas of enhanced growth, or growth 'hot spots', for juvenile walleye pollock and survival may be enhanced when fish overlap with these areas. This study provides evidence that a spatial mismatch between juvenile walleye pollock and growth 'hot spots' in 2005 contributed to poor recruitment while a higher degree of overlap in 2010 resulted in improved recruitment. Our results indicate that climate-driven changes in prey quality and composition can impact growth of juvenile walleye pollock, potentially severely affecting recruitment variability.