Eastern Bering Sea Assessment - 2021

Ecosystem Assessment (pdf)

Elizabeth Siddon

Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA Fisheries Contact: elizabeth.siddon@noaa.gov

Last updated: November 2021

Current Conditions: 2021

During 2021, continued COVID-related data loss impacted research efforts and had a moderate impact on information used in this report. Examples of data loss include survey cancellations, lab processing delays due to limited building access over the past year, and data processing delays due to survey logistics. Similar to 2020, NOAA scientists, state/university partners, tribal governments, and coastal community members provided contributions to mitigate these losses. Nevertheless, these interruptions to data acquisition in 2020 and 2021 provide evidence of the increase in uncertainty when data streams are interrupted and of the importance of a robust, uninterrupted data acquisition program.

It takes Two to Tango: Sea-ice dynamics are driven by both temperature and winds.

Protracted Warmth
Beginning in approximately 2014, the eastern Bering Sea (EBS) entered a warm phase of unprecedented duration (Figures 25 and 30). The EBS remains in this warm phase, though to a lesser degree compared to the extreme years of 2018 and 2019. Sea-ice formation in fall of 2020 was delayed due to residual warmth in the system, which has become the `new normal' during this protracted warm phase. Delayed freeze-up leads to shortened ice seasons that has impacts on ice thickness, ice algae, and thermal modulation as well as impacts to transportation and subsistence activities. While the areal extent of sea ice over the Bering Sea (western and eastern) in winter 2020-2021 was closer to the pre-2014 levels than at any point in the last 7 years (Report Card, Figure 1), over the eastern shelf the ice thickness differed between the northern (thicker ice) and southern (thinner/no ice) regions due to opposing prevailing winds (Physical Environment Synthesis, p. 37).

Tracking the seasonal progression and retreat of sea ice over the shelf highlights the interactive roles of water temperature (i.e., residual warmth in the system) and winds. Atmospheric conditions can have a strong influence on sea surface temperature and ice formation. Wind patterns in February 2021 highlight the decoupling of ecosystem dynamics between the northern and southern Bering Sea. Over the northern shelf, cold northerly winds prevailed and contributed to ice formation and stability/thickness. Over the southern shelf, warm southerly winds prevailed that contributed to reduced sea ice (Figure 20).

Bottom temperatures and Cold Pool
Summer bottom temperatures varied spatially over the shelf. The northern Bering Sea (NBS) shelf bottom waters were very warm in the inner domain with an area of cold bottom waters over the middle domain to the southwest of St. Lawrence Island. The southern shelf had moderately warm bottom water conditions (Figure 35). The summer 2021 cold pool remained significantly reduced in area and its southern boundary was shifted northwestward. The areal extent of the cold pool has increased since 2018, yet the 2021 extent was the 4th lowest on record and remains more than one standard deviation below the mean (Report Card, Figure 1).

Ecosystem Impacts

Northern Bering Sea
Following two winters (2017/2018 and 2018/2019) of little sea ice in the NBS, and two summers (2018 and 2019) of reduced cold pool extent, ecosystem-wide shifts were observed. NOAA bottom trawl surveys indicate northward shifts in the distribution of groundfish species since 2017. Concerns about the food web dynamics and carrying capacity of the NBS have existed since 2018, highlighted by the gray whale Unusual Mortality Event and short-tailed shearwater mass mortality event. Lagged (delayed) impacts of poor feeding conditions experienced during 2018 may partially explain these mortality events. Both species feed in the Bering Sea during summer; gray whales feed in the northern Bering and Chukchi seas and are benthic feeders (e.g., amphipods, crab larvae) while shearwaters are planktivorous (e.g., euphausiids). Both species embark on long migrations south for breeding. The 2019 mortality events may re ect 2018 feeding conditions in the Bering Sea, conditions experienced during the breeding season, or lack of available prey to complete the migration to the Bering Sea in 2019.

In 2021, multiple ecosystem `red flags' occurred in the NBS: (1) crab population declines (p. 145), (2) salmon run failures in the Arctic-Yukon-Kuskokwim region (p. 26), and (3) seabird die-offs combined with low colony attendance and poor reproductive success (p. 147). In addition, (4) results from the 2021 NOAA bottom trawl survey demonstrate a substantial drop in total CPUE in the NBS between 2019 and 2021 that reflected large decreases in all of the dominant species, including pollock (p. 162). Although the collapses are coincident, the underlying mechanisms, or suite of mechanisms, resulting in the collapses reflect cumulative dynamics over the last few years. The mechanisms are not fully understood, but a common thread in these collapses is the marine environment in the NBS, which underwent an abrupt and dramatic change starting in late 2017. A brief discussion of possible mechanisms is provided below under \What Happened in the Northern Bering Sea?".

In 2018, more than 50% of Pacific cod biomass in the EBS was found over the northern portion of the shelf. The northward movement of Pacific cod, among other stocks, into the NBS altered the food web through predation pressure as well as fishery dynamics. For example, the impact of Pacific cod predation on snow crab is one hypothesis that may partially explain the decline in snow crab observed in 2021 (Szuwalski (2021)). It is worth noting here that, at this time, there is no evidence that ocean acidification can be linked to recent declines in surveyed snow crab and red king crab populations (see p. 179 for more on ocean acidification).

Corresponding northward shifts in fishing vessel activity and an increased harvest of Pacific cod in the northern regulatory areas occurred from 2016 through 2020. As the fishing fleet shifted northward following the fish, patterns in groundfish discards also shifted. Fixed gear discards in the NBS trended upward from 2016-2018 as some vessels targeting Pacific cod moved their fishing activity northward; these increases were offset by declines in discard biomass in the southern portion (p. 190). Notably, the first reported interaction between fishing vessels from the BSAI groundfish fishery with threatened spectacled eider may be a direct result of this abrupt ecological change (p. 196), as fishing vessels increase in areas near spectacled eider designated critical habitat.

Total CPUE of all fish and major invertebrate taxa sampled during the 2021 NOAA bottom trawl survey decreased in both the northern and southern portions of the survey (p. 162). In the NBS, CPUE increased between 2010 and 2019, but decreased substantially between 2019 and 2021 (Figure 95). Total CPUE in the southern portion decreased between 2019 and 2021 to the lowest level since 2009. The center of gravity for the groundfish community (p. 168) shifted to the north and into shallower water between 2014-2019 with a substantial shift to the northwest in 2016. The groundfish community distribution shifted slightly to the south in 2017, but remained near its northern maximum through 2019. Between 2019 and 2021, the mean distribution across species shifted back to the southeast again (Figure 102).

What Happened in the Northern Bering Sea?
The coincident collapses in the NBS reflect conditions experienced in the marine environment over the last few years. Researchers will continue to investigate possible mechanistic explanations, but some linkages across these collapses may help inform the need for near-term precautionary management decisions. The current protracted warm phase has resulted in cumulative impacts of increased thermal exposure and metabolic demands. Such multi-year stress means population declines observed in 2021 may be the result of impacts occurring over previous years. For example, the lack of a cold pool in 2018 and 2019, and subsequent northward shift of Pacific cod into the NBS, have been proposed as explanations for the snow crab decline observed in 20213.

Similarly, salmon run failures in the Arctic-Yukon-Kuskokwim Region included Chinook, chum, and coho salmon (p. 26). The 2021 salmon runs were impacted by environmental conditions over multiple years based on life history strategies, including ocean years 2016-2020 for Chinook salmon, 2017-2020 for chum salmon, and 2020 for coho salmon (Figure 5). Several juvenile salmon abundance indices can be used to forecast future run sizes. Juvenile Chinook salmon abundance in the NBS was below average in 2021 and has been below average since 2017 (p. 117). The juvenile pink salmon index, which is generally higher in warmer years, decreased dramatically in 2021 (p. 119). A new indicator based on juvenile chum salmon may be used to forecast adult returns. However, uncertainty in the current juvenile to adult relationship precludes reliable forecasts until additional years of returns are observed (p. 121). In contrast, the 2021 Bristol Bay inshore run of 67.7 million sockeye salmon is the largest on record since 1963 (Figure 64). The large 2021 sockeye salmon run suggests these stocks experienced positive conditions at entry into the EBS in the summers of 2018 and 2019, and winters of 2018-2019 and 2019-2020 (p. 115).

The loss of sea ice during the current protracted warm phase has impacted water column stratification and the vertical distribution of prey (p. 106). Historically, salinity and temperature contribute equally to the vertical stratification of the water column in the NBS. Without increased salinities due to brine rejection as ice forms, the lack of salinity structure results in weaker vertical stratification, permitting greater vertical mixing. If primary and secondary production is mixed deeper in the water column, a vertical mismatch of prey for surface-foraging seabirds or juvenile salmon may limit prey availability, thus exacerbating increased metabolic demands under increased thermal conditions.

The protracted warmth in the NBS, with an increased frequency and duration of marine heatwaves from fall 2017 through winter 2019 (Watson, 2020), and shifts in species distributions (p. 162) has led to concerns about the food web dynamics and carrying capacity of the NBS. Ecosystem response to the 2014-2016 marine heatwave in the Gulf of Alaska resulted in abrupt changes across multiple trophic levels and there were indications the post-marine heatwave system had reduced resiliency (Suryan et al., 2021). Resiliency existed in `functional redundancy' - an example being the ability to switch prey - and without that bufr, ecosystem components could not recover from the marine heatwave perturbation. Evidence of prey switching has been observed in seabirds (i.e., least and crested auklets, p. 147), age-0 pollock in the southeastern Bering Sea, and in the diet of Pacific cod in the southeastern Bering Sea reflecting changes in prey availability. For example, in the southeast middle domain, pollock were the dominant prey of Pacific cod in most years, but when pollock abundance was low from 2008-2012, pollock were replaced in Pacific cod diets with a mix of Chionoecetes spp. and flatfish. Can ecosystem reorganization keep pace with the rate of environmental changes?

Southeastern Bering Sea
Impacts of the loss of sea ice include increases in water temperature (i.e., lack of cold pool), decreases in ice-associated algae, and increases in salinity, and subsequent changes in water density and water column stratification (p. 57). Community-led monitoring of temperature and salinity on St. Paul Island shows an increasing trend in salinity since 2014 (Figure 32). The long-term increase in water density at St. Paul Island is driven primarily by the increase in salinity (Figure 33). Salinity variability on the shelf is driven by ice melt and advection, river discharge, precipitation, evaporation, in flows from the Gulf of Alaska, and cross-slope exchanges with the basin.

Water density and water column stratification can impact the vertical distribution of organisms, including age-0 fish. Age-0 pollock appear to occur deeper in the water column during colder years and closer to the surface during warmer years (p. 106), affecting their availability to predators. In 2021, age-0 pollock may therefore have occurred higher in the water column. Visual predators, such as seabirds, however, may have had reduced foraging success due to a coccolithophore bloom over the southern shelf (Figure 48). The coccolithophore bloom index remained above average in 2021 (p. 87).

Chlorophyll-a biomass, an indicator of primary productivity over the shelf (p. 80), was low along the shelf-break, continuing that trend since 2014 (i.e., start of current protracted warm phase; Figure 44). Along-shelf winds through 2021 were variable and did not consistently demonstrate upwelling or downwelling favorable conditions (Figure 23). Summer 2021 primary production as measured at mooring M2 appeared to be higher than in previous years (2016, 2017, 2019), but lower than in 2018 (p. 85). Secondary production of zooplankton was assessed in spring along the 70-m isobath (p. 94). Small copepod abundance was slightly reduced, although within historical ranges, therefore unlikely to impact food availability for larval fish. Large copepods are less critical in the spring, but very important by fall. Observations of Calanus spp. suggest they were developing more slowly due to the relative colder temperatures, which would result in an increased availability later in the year and potentially support increased overwinter success for age-0 pollock (p. 94).

Species guilds are grouped by functional roles within the ecosystem and trends inform dynamics across these roles (i.e., predation pressure, prey availability) (Report Card, Figure 1). Motile epifauna, which indicate benthic productivity, remained above their long term mean in 2021. Aboveaverage biomass of brittle stars, sea stars, and other echinoderms ofset below-average biomass for all crab functional groups. Benthic foragers were at their lowest level over the times series and indirectly indicate availability of infauna (i.e., prey of these species). A new guild comprised of small forage fishes describes available prey for seabirds and larger fish (i.e., adult pollock). This aggregate forage fish guild indicates a decline in the availability of forage species to predators that may have contributed to other substantial ecosystem changes in the southeastern Bering Sea. In 2021, pelagic foragers, largely driven by adult pollock biomass, dropped to their second lowest value over the time series. Trends indicate availability of forage fish as well as predator abundance within the ecosystem. With the exception of Pacific herring, the 2021 index for all other species and functional groups in the pelagic forager guild were below their long-term means. Togiak herring are an important prey species for piscivorous fish, seabirds, and marine mammals. The high Prohibited Species Catch in the pollock fishery in 2020 supports a strong increase in young EBS herring, as does preliminary Togiak herring data from 2021 (p. 108). Apex predators, largely driven by adult Pacific cod, are below their long term mean in 2021.

For groundfish in the southeastern Bering Sea, bioenergetic indices estimated through 2019 point towards continued increases in thermal exposure and a resulting increase in metabolic demands, as well as declines in foraging and growing conditions (p. 131). For juvenile and adult pollock and Pacific cod, metabolic requirements for prey increased between 2015-2019 relative to historical (1982-2010) rates. Meanwhile, the relative foraging rates for juvenile pollock and Pacific cod declined markedly. Of particular note, from 2015-2019 juvenile Pacific cod scope for growth remained well below the long-term average (1982-2010) (Figure 77). Fish condition, as measured by lengthweight residuals, trended downward from 2019 to 2021 for multiple groundfish species, including benthic, pelagic, and apex predators (Figure 72), indicating poor feeding conditions across trophic niches. Conversely, juvenile pollock (100-250 mm) condition has trended upward since 2017, indicating positive bottom-up drivers. Additionally, based on results from the multispecies model CEATTLE (p. 136), juvenile pollock experienced improved top-down conditions through predation release (i.e., due to declining biomass of groundfish predators) (Figure 79).

Complete Recap of the 2020 Ecosystem State

Some ecosystem indicators are updated to the current year (2021), while others can only be up- dated to the previous year (or earlier) due to the nature of the data collected, sample processing, or modeling efrts. Therefore, some of the \new" updates in each Ecosystem Status Report reflect information from the previous year(s). Below is a complete summary of 2020 that includes information from both previous and current indicators.

During 2020, the vast majority of NOAA Fisheries surveys were canceled in the eastern and northern Bering Sea due to COVID-19 travel restrictions. 2020 was an on-year for the biennial NOAA ecosystem and acoustics surveys, in addition to annual trawl surveys. Therefore numerous contributions of ecosystem information for this Report were unable to be updated last year. Due to these survey limitations, the interpretation of the ecosystem state bridged from basin-scale, satellitederived indicators to local-scale community observations. While gaps existed, NOAA scientists, state/university partners, tribal governments, and coastal community members provided new and innovative contributions to inform our understanding of the ecosystem status. For example, coastal community members, tribal governments, and state/university partners provided all information on seabird dynamics in 2020 and the U.S. Fish and Wildlife Service biologists helped to synthesize the information and provide implications.

Following two years of physical oceanographic perturbations, the EBS experienced a return to nearnormal climatic conditions in 2020. The winters of 2017/2018 and 2018/2019 had unprecedentedly low sea ice and reduced spatial extent of the cold pool, removing the thermal barrier between the southern and northern Bering Sea shelves. Distributional shifts in groundfish stocks were observed (e.g., more than 50% of the overall biomass of Pacific cod biomass occurred in the NBS in 2018). Ecosystem impacts in response to these conditions include changes in overall productivity and the potential for new trophic pathways.

Considerable cooling during winter 2019/2020 allowed for rapid build-up of sea ice, exceeding median ice extent in parts of February and March 2020. However, ice thickness was low, and retreated quickly in spring. Based on Bering 10K Regional Ocean Modeling System (ROMS) hindcast simulation, this ephemeral ice was estimated to be suffcient to form a cold pool of average spatial extent. After two years of little to no sea ice over the Bering Sea shelf, the near-normal ice extent observed in 2020 appeared to have only minimal mitigating effects on the warmth in the upper water column (i.e., sea surface temperatures). This vertical stratification of the water column is more typical of shelf conditions and affects predator/prey dynamics.

Above-average sea surface temperatures returned in spring 2020 and remained above average through summer 2020. Satellite-derived indicators of sea surface temperature (SST) facilitated examination of marine heatwave thresholds for the EBS. Heatwaves occurred during early years of the time series that begins in 1985, but the frequency and duration of heatwaves have increased dramatically, especially in the NBS, where residual heat and low sea ice extent has resulted in significantly increased cumulative annual thermal exposure since 2017.

Chlorophyll-a concentrations were lower in 2020 than 2019 in all regions except the southern outer domain. Chl-a concentrations over the southern inner and middle shelves had been below average since 2016. In the NBS, the concentrations over the inner and middle shelves were below average and the outer shelf was low and continued a decreasing trend since 2014. Primary producers provide fundamental energy and nutrients for zooplankton grazers and higher trophic level species; these trends indicate lower energy transfer to support the food web over the southern and northern Bering Sea shelves in 2020. The timing of the peak spring bloom in 2020 was earlier than the long-term average; for the southern inner and middle shelves it occurred about a week earlier. This contrasts with 2018 which was among the latest, while 2017 was among the earliest spring blooms. New information derived from the Continuous Plankton Recorder (p. 91) shows that the copepod community size and mesozooplankton biomass anomalies for 2020 were negative, where they had been positive in 2019. The mean diatom abundance anomaly was also negative in 2020. Such changes in abundance or biomass, together with size of the copepod community, in uences the quantity and quality of prey available to predators. The coccolithophore bloom index was below average in 2018 and 2019 but increased, particularly on the middle shelf, in 2020. Coccolithophores may be a less desirable food source for microzooplankton in this region and smaller coccolithophores result in longer trophic chains. The striking milky aquamarine color of the water during a coccolithophore bloom can also reduce foraging success for visual predators. Combined, these indicators of primary production suggest limited and/or poor quality of the prey base to support trophic energy transfer (e.g., juvenile fish, seabirds) in 2020.

The 2020 Togiak herring population was predominantly comprised of age-6 and age-7 fish (the 2013 and 2014 year classes). Oceanographic conditions over the southeastern Bering Sea shelf transitioned from below-average (i.e., cold) in 2013 to above-average (i.e., warm) in 2014. While the recruitment of age-4 fish to the spawning population in 2018 was still the largest estimated recruitment since 1982, the magnitude of that recruit class was estimated in the 2020-forecast model to be lower than was previously estimated. The incidental catch of herring in the 2020 directed pollockfishery was unusual because it occurred during a period of relatively high nominal CPUE values for pollockfishing and also was highest in the winterfishing A season. Several hypotheses were explored in the Noteworthy \Incidental Catch of Herring in groundfish Fisheries Increased in 2020" in Siddon et al. (2020); the pollock eet may have encountered high numbers of Togiak age-4 fish that provides partial explanation of the abrupt increase of incidental catch in 2020.

Commercial salmon harvests in 2020, based on preliminary data from ADF&G, indicated that statewide total harvests were below the preseason forecast, but nearing the 2018 total harvest. The 2020 Bristol Bay salmon inshore run was the 5th largest on record and 74.5% higher than the 1963{2019 average. A projected decrease in the number of pink salmon in 2020 may have had a positive impact on fish-eating seabirds (i.e., less competition for prey).

In 2020, at the Pribilof Islands, seabird attendance appeared similar to that in recent years while breeding observations suggested it was an average, to slightly below average, year for most fisheating species (e.g., kittiwakes, murres). Planktivorous species (i.e., auklets) had been declining and continued to be low in 2020, at least at St. Paul Island. Warmer water temperatures from 2014{2019 seem to have negatively affected least auklets, and likely parakeet auklets. In the NBS, on St. Lawrence Island, reproductive success and colony attendance differed among fish-eating and planktivorous seabirds suggesting foraging impacts differed across trophic levels. In the Bering Strait region, emaciation and starvation were observed in some seabirds throughout the summer and beach-cast carcasses of several species of seabirds were observed on the eastern and western sides of the Bering Strait.

Seabird bycatch estimates from the groundfishfisheries (p. 196) decreased 52% from 2019 to 2020. While a reduction in seabird bycatch in the Federalfisheries off Alaska is positive, several events occurred during the 2020fishing seasons which may partially explain this reduction: (i) the COVID-19 pandemic disrupted normalfishing operations throughout Federal Fisheries, including lostfishing days; (ii) an expansion of the eet over space (i.e., into the NBS), and (iii) reductions in catch over time (e.g., from 247,000 t in 2016 to ≈150,000 t in 2020). Additionally, the first reported interaction between afishing vessel from the BSAI groundfish fishery with threatened spectacled eider may be a direct result of ecological change in the EBS. Recent changes in ocean temperatures and the resulting ecological response of commercially valuable fish species, mainly Pacific cod, has led to an increase in the amount offishing vessel traffic in areas near spectacled eider designated critical habitat.

Direct and indirect indicators of groundfish recruitment success provided information on the status of 2020 year classes. The 2020 springtime drift pattern was mixed, indicating larvae (e.g., age-0 pollock) may have been retained over the southern middle shelf. However, lower primary production in spring 2020 may have limited the prey base to support trophic energy transfer to large, lipidrich copepod taxa. The abundance of large copepods is positively correlated with the recruitment success of pollock. Years of low recruitment for pollock portend lower rates of cannibalism as adult pollock biomasses decreases. The climate-enhanced multispecies model (CEATTLE) estimates of age-1 predation mortality for pollock was at the long-term mean in 2020 as declines in total predator biomass are contributing to reduced predation rates and mortality. 15