Investigation of Algal Toxins in a Multispecies Seabird Die-Off in the Bering and Chukchi Seas.

Between 2014 and 2017, widespread seabird mortality events were documented annually in the Bering and Chukchi seas, concurrent with dramatic reductions of sea ice, warmer than average ocean temperatures, and rapid shifts in marine ecosystems. Among other changes in the marine environment, harmful algal blooms (HABs) that produce the neurotoxins saxitoxin (STX) and domoic acid (DA) have been identified as a growing concern in this region. Although STX and DA have been documented in Alaska (US) for decades, current projections suggest that the incidence of HABs is likely to increase with climate warming and may pose a threat to marine birds and other wildlife. In 2017, a multispecies die-off consisting of primarily Northern Fulmars (Fulmarus glacialis) and Short-tailed Shearwaters (Ardenna tenuirostris) occurred in the Bering and Chukchi seas. To evaluate whether algal toxins may have contributed to bird mortality, we tested carcasses collected from multiple locations in western and northern Alaska for STX and DA. We did not detect DA in any samples, but STX was present in 60% of all individuals tested and in 88% of Northern Fulmars. Toxin concentrations in Northern Fulmars were within the range of those reported from other STX-induced bird die-offs, suggesting that STX may have contributed to mortalities. However, direct neurotoxic action by STX could not be confirmed and starvation appeared to be the proximate cause of death among birds examined in this study.

Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Heatwave-induced synchrony within forage fish portfolio disrupts energy flow to top pelagic predators.

During the Pacific marine heatwave of 2014-2016, abundance and quality of several key forage fish species in the Gulf of Alaska were simultaneously reduced throughout the system. Capelin (Mallotus catervarius), sand lance (Ammodytes personatus), and herring (Clupea pallasii) populations were at historically low levels, and within this community abrupt declines in portfolio effects identify trophic instability at the onset of the heatwave. Although compensatory changes in age structure, size, growth or energy content of forage fish were observed to varying degrees among all these forage fish, none were able to fully mitigate adverse impacts of the heatwave, which likely included both top-down and bottom-up forcing. Notably, changes to the demographic structure of forage fish suggested size-selective removals typical of top-down regulation. At the same time, changes in zooplankton communities may have driven bottom-up regulation as copepod community structure shifted toward smaller, warm water species, and euphausiid biomass was reduced owing to the loss of cold-water species. Mediated by these impacts on the forage fish community, an unprecedented disruption of the normal pelagic food web was signaled by higher trophic level disruptions during 2015-2016, when seabirds, marine mammals, and groundfish experienced shifts in distribution, mass mortalities, and reproductive failures. Unlike decadal-scale variability underlying ecosystem regime shifts, the heatwave appeared to temporarily overwhelm the ability of the forage fish community to buffer against changes imposed by warm water anomalies, thereby eliminating any ecological advantages that may have accrued from having a suite of coexisting forage species with differing life-history compensations.

Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016.

About 62,000 dead or dying common murres (Uria aalge), the trophically dominant fish-eating seabird of the North Pacific, washed ashore between summer 2015 and spring 2016 on beaches from California to Alaska. Most birds were severely emaciated and, so far, no evidence for anything other than starvation was found to explain this mass mortality. Three-quarters of murres were found in the Gulf of Alaska and the remainder along the West Coast. Studies show that only a fraction of birds that die at sea typically wash ashore, and we estimate that total mortality approached 1 million birds. About two-thirds of murres killed were adults, a substantial blow to breeding populations. Additionally, 22 complete reproductive failures were observed at multiple colonies region-wide during (2015) and after (2016-2017) the mass mortality event. Die-offs and breeding failures occur sporadically in murres, but the magnitude, duration and spatial extent of this die-off, associated with multi-colony and multi-year reproductive failures, is unprecedented and astonishing. These events co-occurred with the most powerful marine heatwave on record that persisted through 2014-2016 and created an enormous volume of ocean water (the "Blob") from California to Alaska with temperatures that exceeded average by 2-3 standard deviations. Other studies indicate that this prolonged heatwave reduced phytoplankton biomass and restructured zooplankton communities in favor of lower-calorie species, while it simultaneously increased metabolically driven food demands of ectothermic forage fish. In response, forage fish quality and quantity diminished. Similarly, large ectothermic groundfish were thought to have increased their demand for forage fish, resulting in greater top-predator demands for diminished forage fish resources. We hypothesize that these bottom-up and top-down forces created an "ectothermic vise" on forage species leading to their system-wide scarcity and resulting in mass mortality of murres and many other fish, bird and mammal species in the region during 2014-2017.

An assessment of climate change vulnerability for Important Bird Areas in the Bering Sea and Aleutian Arc.

Recently available downscaled ocean climate models for the Bering Sea and Aleutian Arc offer the opportunity to assess climate vulnerability for upper trophic level consumers such as marine birds. We analyzed seasonal and annual spatial projections from three climate models for two physical climate variables (seawater temperature and sea ice) and three forage variables (large copepods, euphausiids, and benthic infauna), comparing projected conditions from a recent time period (2003-2012) to a future time period (2030-2039). We focused the analyses on core areas within globally significant Important Bird Areas, and developed indices of the magnitude of projected change and vulnerability agreement among models. All three climate models indicated a high degree of change for seawater temperature warming (highest in the central and eastern Aleutian Islands) and ice loss (most significant in the eastern Bering Sea) across scales, and we found those changes to be significant for every species and virtually every core area assessed. There was low model agreement for the forage variables; while the majority of core areas were identified as climate vulnerable by one or more models (72% for large copepods, 73% for euphausiids, and 94% for benthic infauna), very few were agreed upon by all three models (only 6% of euphausiid-forager core areas). Based on the magnitude-agreement score, euphausiid biomass decline affected core areas for fulmars, gulls, and auklets, especially along the outer shelf and Aleutian Islands. Benthic biomass decline affected eiders along the inner shelf, and large copepod decline was significant for storm-petrels and auklets in the western Aleutians. Overall, 12% of core areas indicated climate vulnerability for all variables assessed. Modeling and interpreting biological parameters to project future dynamics remains complex; the strong signal for projected physical changes raised concerns about lagged responses such as distribution shifts, breeding failures, mortality events, and population declines.

Timing of ice retreat alters seabird abundances and distributions in the southeast Bering Sea.

Timing of spring sea-ice retreat shapes the southeast Bering Sea food web. We compared summer seabird densities and average bathymetry depth distributions between years with early (typically warm) and late (typically cold) ice retreat. Averaged over all seabird species, densities in early-ice-retreat-years were 10.1% (95% CI: 1.1-47.9%) of that in late-ice-retreat-years. In early-ice-retreat-years, surface-foraging species had increased numbers over the middle shelf (50-150 m) and reduced numbers over the shelf slope (200-500 m). Pursuit-diving seabirds showed a less clear trend. Euphausiids and the copepod Calanus marshallae/glacialis were 2.4 and 18.1 times less abundant in early-ice-retreat-years, respectively, whereas age-0 walleye pollock Gadus chalcogrammus near-surface densities were 51× higher in early-ice-retreat-years. Our results suggest a mechanistic understanding of how present and future changes in sea-ice-retreat timing may affect top predators like seabirds in the southeastern Bering Sea.

A spatial-seasonal analysis of the oiling risk from shipping traffic to seabirds in the Aleutian Archipelago.

Some of the largest seabird concentrations in the northern hemisphere are intersected by major shipping routes in the Aleutian Archipelago. Risk is the product of the probability and the severity incidents in an area. We build a seasonally explicit model of seabird distribution and combine the densities of seabirds with an oil vulnerability index. We use shipping density, as a proxy for the probability of oil spills from shipping accident (or the intensity chronic oil pollution). We find high-risk (above-average seabird and vessel density) areas around Unimak Pass, south of the Alaska Peninsula, near Buldir Island, and north of Attu Island. Risk to seabirds is greater during summer than during winter, but the month of peak risk (May/July) varies depending on how data is analyzed. The area around Unimak Pass stands out for being at high-risk year-round, whereas passes in the western Aleutians are at high risk mostly during summer.

Prey patch patterns predict habitat use by top marine predators with diverse foraging strategies.

Spatial coherence between predators and prey has rarely been observed in pelagic marine ecosystems. We used measures of the environment, prey abundance, prey quality, and prey distribution to explain the observed distributions of three co-occurring predator species breeding on islands in the southeastern Bering Sea: black-legged kittiwakes (Rissa tridactyla), thick-billed murres (Uria lomvia), and northern fur seals (Callorhinus ursinus). Predictions of statistical models were tested using movement patterns obtained from satellite-tracked individual animals. With the most commonly used measures to quantify prey distributions--areal biomass, density, and numerical abundance--we were unable to find a spatial relationship between predators and their prey. We instead found that habitat use by all three predators was predicted most strongly by prey patch characteristics such as depth and local density within spatial aggregations. Additional prey patch characteristics and physical habitat also contributed significantly to characterizing predator patterns. Our results indicate that the small-scale prey patch characteristics are critical to how predators perceive the quality of their food supply and the mechanisms they use to exploit it, regardless of time of day, sampling year, or source colony. The three focal predator species had different constraints and employed different foraging strategies--a shallow diver that makes trips of moderate distance (kittiwakes), a deep diver that makes trip of short distances (murres), and a deep diver that makes extensive trips (fur seals). However, all three were similarly linked by patchiness of prey rather than by the distribution of overall biomass. This supports the hypothesis that patchiness may be critical for understanding predator-prey relationships in pelagic marine systems more generally.