On the temporal variability of the physical environment over the south-eastern Bering Sea

During 1997 and 1998, unusual physical conditions occurred in the Bering Sea: strong May storms and calm conditions in July; record high sea surface temperature; a shallow wind mixed layer; a fresher-than-normal water column; and abnormal cross-shelf currents. Accompanying these conditions were changes in the dominant phytoplankton, a die-off of seabirds, increased sightings of large whales and diminished returns of salmon. Changes to the physical environment during 1997 and 1998 are placed in context of historical meteorological and oceanographic data sets. Although 1997 had the warmest sea surface temperature ever observed on the south-east Bering Sea shelf, the heat content of the water column was cooler than average. In contrast, during 1998, the sea surface temperature was cooler than in 1997 but the water column had significantly higher heat content. During recent years, the water column has freshened over the middle shelf because of increased sea ice and reduction of on-shelf transport of the saline, high-nutrient water from the slope. The timing of the spring bloom is directly related to the presence of ice. When ice is advected over the south-east shelf during March/April an early, sharp phytoplankton bloom occurs. The absence of ice during this critical time is associated with a May/June bloom.     

Anomalous conditions in the south-eastern Bering Sea, 1997: nutrients, phytoplankton and zooplankton

Anomalies in the regional weather over the south-eastern Bering Sea during spring and summer of 1997 resulted in significant differences in nutrient availability, phytoplankton species composition, and zooplankton abundance over the continental shelf as compared with measurements in the 1980s. Calm winds and the reduction of cloud cover in spring and summer produced a very shallow mixed layer in which nitrate and silicate were depleted after an April diatom bloom. High submarine light levels allowed subsequent phytoplankton growth below the pycnocline and eventual depletion of nitrate from the water column to depths of 70 m or more. Thus, total new production during 1997 may have exceeded that of previous years when nitrate was not depleted below the pycnocline. A bloom of the coccolithophorid, Emiliania huxleyi , was observed in early July in the warm, nutrient-depleted waters over the middle and inner shelf. Emiliania huxleyi concentrations reached 4.5 × 10⁶ cells L^–1 by September, and the bloom persisted through the autumn. There was evidence for increased abundance of some species of copepods in 1997 as compared with data from the middle domain in June 1981. The abundance of adult and juvenile euphausiids in 1997 was statistically similar to values measured in 1980 and 1981. However, near-surface swarms were rarely observed on the inner shelf in August–September 1997. Lack of euphausiid availability in the upper water column may partially explain the August–September mass mortality of planktivorous short-tailed shearwaters ( Puffinus tenuirostris ) observed on the inner shelf.     

Anomalous conditions in the south-eastern Bering Sea 1997: linkages among climate, weather, ocean, and Biology

In 1997, the Bering Sea ecosystem, a productive, high-latitude marginal sea, demonstrated that it responds on very short time scales to atmospheric anomalies. That year, a combination of atmospheric mechanisms produced notable summer weather anomalies over the eastern Bering Sea. Calm winds, clear skies, and warm air temperatures resulted in a larger-than-normal transfer of heat to surface waters and the establishment of a shallow mixed layer. In spring, significant new production occurred below the shallow pycnocline over the Middle Shelf, depleting the subpycnocline nutrient reservoir that normally exists during summer. Following the depletion of nitrate and silicate from the system, a sustained (≥ 4 months) bloom of coccolithophores ( Emiliania huxleyi ) was observed – a phenomenon not previously documented in this region. Summer Middle Shelf Domain copepod concentrations were higher for some species in 1997 than in the early 1980s. Warmer surface water and lack of wind mixing also changed the basic distribution of hydrographic regimes on the south-eastern shelf and altered the strength and position of fronts or transition zones where apex predators seek elevated food concentrations. The Inner Front was well inshore of its normal position, and adult euphausiids (the primary prey of short-tailed shearwaters, Puffinus tenuirostris ) were unavailable at, and shoreward of, the front in autumn. High shearwater mortality rates followed the period of low euphausiid availability. Some, but not all, of these anomalous conditions re-occurred in 1998. These observations are another demonstration that the structure and function of marine ecosystems are intimately tied to forcing from the atmosphere. Alteration of climatological forcing functions, expressed as weather, can be expected to have large impacts on this ecosystem and its natural resources.     

Body size trends along vertical and thermal gradients of chum salmon in the Bering Sea during summer

Relationships between the vertical distribution and thermal habitat, and body size of chum salmon Oncorhynchus keta were studied in the Bering Sea in summer using trawl surveys at various depths. Chum salmon abundance decreased with increasing depth, but the patterns of decrease differed between size groups. The abundance of small salmon fell rapidly with depth, whereas that of large salmon decreased gradually to 40 m depth, and abruptly below that. The average fork length of chum salmon collected from each trawl correlated positively with trawl net depth and negatively with water temperature. Since the optimal temperature for growth decreases with body size in this species, the observed body size‐related vertical habitat use by chum salmon may indicate size‐dependent thermal preferences.     

Early- to late-summer population growth and prey consumption by age-0 pollock (Theragra chalcogramma), in two years of contrasting pollock abundance near the Pribilof Islands, Bering Sea

Acoustic survey data were used to estimate the abundance and distribution of age-0 walleye pollock and zooplankton near the Pribilof Islands, Bering Sea, nursery area at two time periods in two consecutive years: the beginning of August, and mid-September, of 1996 and 1997. The 1996 pollock year class ultimately produced a large adult cohort in the eastern Bering Sea, while the 1997 year class produced a below-average adult cohort. Acoustic densities of age-0 pollock were significantly lower in August – and declined more strongly from August to September – in 1997 than in 1996, indicating that the trend to adult cohort strength was already set by August. Diet composition analyses revealed that age-0 pollock ate a much higher proportion of euphausiids in 1997 than in 1996, despite lower acoustic abundance of euphausiids in 1997. We infer that in 1996, age-0 pollock experienced greater feeding success by August, with high concentrations of copepods available for smaller fish to consume, and high concentrations of euphausiids available for larger individuals. In 1997, age-0 pollock had lower body condition in August and may have been limited by the availability of small (<2 mm) copepods. Bioenergetic modeling of prey consumption did not indicate a likelihood that age-0 pollock would begin to deplete euphausiids until late August in 1996, and not at all between August and mid-September in 1997.     

Spatial and temporal patterns in summer ichthyoplankton assemblages on the eastern Bering Sea shelf 1996–2007

Larval and early juvenile fishes were sampled from the eastern Bering Sea (EBS) shelf from 2001 to 2005, and in 2007. Data from these collections were used to examine spatial and temporal patterns in species assemblage structure and abundance. The years 2001–2005 were unusual because the EBS water temperature was ‘warm’ compared with the long‐term mean temperature. In contrast, 2007 was a ‘cold’ year. The abundance of the five most numerous taxa at 12 stations common to all years sampled (1996–2005, 2007) were significantly different among years. Larval and early juvenile stage Theragra chalcogramma (walleye pollock), a commercially important gadid, were by far the most abundant fish in all years. Bottom depth alone best explained assemblage structure in most years, but in others, bottom depth and water column temperature combined and percent sea‐ice coverage were most important. Abundance of T. chalcogramma larvae increases with water column temperature until 5°C and then becomes level. Higher abundances of Gadus macrocephalus (Pacific cod) larvae occur in years with the greatest percent sea‐ice cover as indicated by GAM analysis. Larvae of Lepidopsetta polyxystra (northern rock sole) increase in abundance with increasing maximum wind speed, but decrease at a later date during the last winter storm. The data are consistent with the hypothesis that oceanographic conditions, specifically water temperature and sea‐ice coverage, affect the spatial and temporal pattern of larval abundances. In general, ichthyoplankton species assemblages can be important early indicators of environmental change in the Bering Sea and potentially other subarctic seas as well.     

Spatial and temporal patterns in summer ichthyoplankton assemblages on the eastern Bering Sea shelf 1996–2000

Larval and early juvenile fishes were sampled from the eastern Bering Sea (EBS) shelf during summer from 1996 to 2000. Data from these collections were used to examine spatial and temporal patterns in species assemblage structure and abundance. Cluster analyses based on Bray–Curtis dissimilarity coefficients were used to group species and stations according to similar abundance and species composition. Ordination techniques were used to verify groupings, and a non‐parametric stepwise procedure using a Spearman correlation coefficient (BIO‐ENV) was used to relate groupings to predominant environmental variables. These approaches revealed a pattern of station groupings that were generally related to bathymetry in 1996, 1997, 1999, and 2000, although no obvious relationship to geographic boundaries was observed in 1998. Significant differences in species associations were observed in 1997 and 1998, and depressions in abundance were also noted among many species between 1997 and 1999. A regional, full primitive equation model was used to simulate float trajectories on the EBS shelf in each year to better relate fish distributional observations to prevailing current patterns. Model results indicated general variations in flow in several years, although 1998 stood out with stronger northeast flow than in any of the other years examined. Observed disruptions of larval and early juvenile fish assemblages could be related to the strong El‐Niño event of 1997–98 in the EBS. If this idea is confirmed, our study suggests that larval and juvenile fish are sensitive and respond relatively quickly (1–2 yr) to environmental perturbations, and as such, may be timely indicators of environmental change.     

Ubiquitous eddies of the eastern Bering Sea and their coincidence with concentrations of larval pollock

Between 1988 and 1993, 12 satellite-tracked buoys were deployed in four eddies in the south-eastern Bering Sea. Our success in finding eddies resulted from placing buoys in high concentrations of walleye pollock (Them-gra chalcogramma) larvae. We utilize data from hydro-graphic surveys, satellite-tracked buoys and moored current meters to describe the eddies. Small (< 25 km diameter) eddies likely transit along the slope of the eastern Bering Sea every 45–60 days. In previous studies such small features were not observed because their size fell within typical separation of hydrographic stations and the weak sea surface temperature gradients are not resolved by satellite-borne infrared imagery.     

The importance of episodic weather events to the ecosystem of the Bering Sea shelf

Climate variability on decadal time scales is generally recognized to influence high‐latitude marine populations. Our recent work in studying air–sea interactions in the Bering Sea suggests that interannual to decadal climate variability is important through its modulation of the frequencies and magnitudes of weather events on intraseasonal time scales. We hypothesize that it is these weather events that directly impact the marine ecosystem of the Bering Sea shelf. The linkages between the event‐scale weather and the ecosystem are illustrated with three examples: walleye pollock (Theragra chalcogramma), Tanner crabs (Chionoecetes bairdi), and coccolithophorid phytoplankton (Emiliania huxleyi). We hypothesize that the strong recruitment of walleye pollock that occurred in 1978, 1982, and 1996 can be attributed in part due to the seasonably strong storms that occurred in the early summer of those years. These storms caused greater than normal mixing of nutrients into the euphotic zone which presumably led to sustained primary productivity after the spring bloom and, possibly, enhanced prey concentrations for pollock larvae and their competitors. Recruitment of Tanner crab was particularly strong for the 1981 and 1984 year‐classes. These years had periods of prominent east wind anomalies along the Alaska Peninsula during the previous winter. Such winds promote flow through Unimak Pass, and hence an enhanced flux of nutrient‐rich water onto the shelf. This mechanism may have ultimately resulted in favorable feeding conditions for Tanner crab larvae. Finally, an unprecedented coccolithophorid bloom occurred over the Bering Sea shelf in the summer of 1997. This summer featured lighter winds and greater insolation than usual after a spring that included a very strong May storm. This combination brought about a warm, nutrient‐poor upper mixed layer by mid‐summer. This provided a competitive advantage for coccolithophorid phytoplankton in 1997 and to a lesser extent in 1998. Unusually high concentrations of coccolithophores persisted for the following two years although physical environmental conditions did not remain favorable. While slow variations in the overall aspects of the physical environment may be important for setting the stage, we propose that the significant multi‐year adjustments in the marine ecosystem of the Bering Sea shelf are more directly caused by major air–sea interaction events on intraseasonal time scales.     

Ontogeny matters: Climate variability and effects on fish distribution in the eastern Bering Sea

Analyses of climate effects often ignore differences in life history for individual species. We analyzed a 34‐year time series of eastern Bering Sea fish surveys to evaluate changes in distribution by length and between cold and warm shelf‐wide average water temperatures for 20 species over inhabited depth, temperature, and location. All species showed evidence of ontogenetic migration. Differences in distribution between years with warm and years with cold shelf‐wide water temperatures varied among species and within species at different lengths. For species where shelf‐wide temperature effects were detected, the mid‐sized fish were most active in changing spatial distribution. For aquatic organisms ontogenetic migration occurs because life history stages have different environmental requirements. This study illustrates the need to consider species responses to climate change over different life history stages, and that studies on ecosystem responses should take ontogenetic differences into consideration when assessing impacts.     

Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change

We examined quantitative catches of large medusae from summer bottom trawl surveys that sampled virtually the same grid station on the eastern Bering Sea shelf using the same methodology every year from 1979 to 1997. This series shows a gradual increase in biomass of medusae from 1979 to 1989, followed by a dramatic increase in the 1990s. The median biomass increased tenfold between the 1982–1989 and 1990–1997 periods. Most of this biomass was found within the Middle Shelf Domain (50 <  z  < 100 m). The greatest rate of increase occurred in the north-west portion of this domain. Whether this dramatic increase in biomass of gelatinous zooplankton has resulted from some anthropogenic perturbation of the Bering Sea environment or is a manifestation of natural ecosystem variability is unclear. However, several large-scale winter/spring atmospheric and oceanographic variables in the Bering Sea exhibited concomitant changes beginning around 1990, indicating that a possible regime change occurred at this time.     

A synthesis of biological and physical processes affecting the feeding environment of larval walleye pollock (Theragra chalcogramma) in the eastern Bering Sea

Biological and physical phenomena that affect conditions for larval survival and eventual recruitment differ in the oceanic and shelf regions. In the oceanic region, eddies are a common feature. While their genesis is not well known, eddies have unique biophysical characteristics and occur with such regularity that they likely affect larval survival. High concentrations of larval pollock often are associated with eddies. Some eddies are transported onto the shelf, thereby providing larvae to the Outer Shelf Domain. Advection, rather than local production, dominated the observed springtime increase in chlorophyll (often a correlate of larval food) in the oceanic region. Over two-thirds of the south-eastern shelf, eddies are absent and other phenomena are important. Sea ice is a feature of the shelf region: its interannual variability (time of arrival, persistence, and areal extent) affects developmental rate of larvae, timing of the phytoplankton bloom (and potentially the match/mismatch of larvae and prey), and abundance and distribution of juvenile pollock. In the oceanic region, interannual variation in food for first-feeding pollock larvae is determined by advection; in the shelf region, it is the coupled dynamics of the atmosphere–ice–ocean system.     

Regime shifts and recruitment dynamics of snow crab,Chionoecetes opilio,in the eastern Bering Sea

Shifts in climate regime are prominent features of the physical environment of the eastern Bering Sea and in recent years have been documented in approximately 1977 and 1989. Average snow crab (Chionoecetes opilio) recruitment decreased sharply after the 1989 fertilization year. Models in which control of snow crab recruitment shifts between drivers dependent on climate ‘regime’ are presented. These models are evaluated using cross‐validation and retrospective analysis, both of which indicate that the relationships are relatively robust to varying levels of information. Larval survival as influenced by food availability in the pelagic phase and advection to suitable nursery grounds are the hypothesized mechanisms driving recruitment dynamics.     

Variation in the distribution of yellowfin sole Limanda aspera larvae in warm and cold years in the eastern Bering Sea

Multiyear periods of relatively cold temperatures (2007–2013) and warm temperatures (2001–2005 and 2014–2018) altered the eastern Bering Sea ecosystem, affecting ocean currents and wind patterns, plankton community, and spatial distribution of fishes. Yellowfin sole Limanda aspera larvae were collected from the inner domain (≤50 m depth) of the eastern Bering Sea among four warm years (2002, 2004, 2005, 2016), an average year (2006), and three cold years (2007, 2010, 2012). Spatial distribution and density of larvae among those years was analyzed using generalized additive models that included timing of sea-ice retreat, areal coverage of water ≤0°C, and water temperature as covariates. Analyses indicated a combination of temperature effects on the location and timing of spawning, and on egg and larval survival, may explain the variation in larval density and distribution among years. During warm years, higher density and wider spatial distribution of larvae may be due to earlier spawning, an expansion of the spawning area, and higher egg and larvae survival due to favorable temperatures. Larval distribution contracted shoreward, and density was lower during cold conditions and was likely due to fish spawning closer to shore to remain in preferred temperatures, later spawning, and increased mortality. Predicted drift trajectories from spawning areas showed that larvae would reach nursery grounds in most years. Years when the drift period was longer than the pelagic phase of the larvae occurred during both warm and cold conditions indicating that settlement outside of nursery areas could happen during either temperature condition.     

Use of juvenile salmon growth and temperature change indices to predict groundfish post age‐0 yr class strengths in the Gulf of Alaska and eastern Bering Sea

Juvenile marine growth (SW1) of salmon and a new temperature change (TC) index were evaluated as ecosystem indicators and predictors for the post age‐0 year class strength (YCS) of groundfish in the Gulf of Alaska (GOA) and eastern Bering Sea (EBS). Our hypothesis was that SW1, as measured on the scales of adult Pacific salmon (Oncorhynchus spp.), is a proxy for ocean productivity on the continental shelf, a rearing area for young salmon and groundfish. Less negative TC index values are the result of a cool late summer followed by a warm spring, conditions favorable for groundfish YCS. In the GOA, SW1 was a positive predictor of age‐1 pollock (Theragra chalcogramma), but not age‐2 sablefish (Anoplopoma fimbria) YCS, indicating that the growth of the Karluk River sockeye salmon that enter Shelikof Strait is a proxy for ocean conditions experienced by age‐0 pollock. Contrary to our hypotheses, the TC index was a negative predictor of GOA pollock YCS; and the SW1 a negative predictor of EBS pollock and cod YCS since the 1980s. Recent fisheries oceanography survey results provide insight into possible mechanisms to support the inverse SW1 and YCS relationship. For the EBS, the TC index was a significant positive predictor for pollock and cod YCS, supporting the hypothesis that a cool late summer followed by a warm spring maximizes the over‐wintering survival of pollock and cod (Gadus macrocephalus), especially since the 1980s. The TC and SW1 index showed value for the assessment of pollock and cod, but not sablefish.     

Distribution and drift pathways of Greenland halibut (Reinhardtius hippoglossoides) during early life stages in the eastern Bering Sea and Aleutian Islands

We describe the spatial distribution and dispersal pathways of Greenland halibut (Reinhardtius hippoglossoides) early life stages based on historical field data from the eastern Bering Sea and adjacent water along the eastern Aleutian Islands. Our results indicate that Greenland halibut from preflexion larvae to newly settled juveniles have a long pelagic duration and are subject to extended drift pathways. Hatching may occur in deep water, below 530 m, and larvae rise in the water column as they grow. Flexion/postflexion larvae are mostly found around the Pribilof Islands over the middle shelf (50–100‐m isobaths) in July, and settling occurs during late summer on the middle shelf near St. Matthew Island. However, given that age‐1 individuals were primarily found on the outer shelf, it appears that Greenland halibut actively move to deeper water with age (or size). The mechanisms of slope–shelf connectivity in preflexion larvae may be related to the Bering Slope Current in the vicinity of both Bering and Pribilof Canyons. This study shows that Greenland halibut early life stages have extensive horizontal ontogenetic migrations in the Bering Sea, and utilize a range of geographic areas over the basin and slope along the Aleutian Islands and in the eastern Bering Sea. Based on these results, it is hypothesized that settlement success and recruitment of Greenland halibut may be influenced by variability in currents and flows of the Bering Sea slope and shelf during their transport.     

Copepod dynamics across warm and cold periods in the eastern Bering Sea: Implications for walleye pollock (Gadus chalcogrammus) and the Oscillating Control Hypothesis

Differences in zooplankton populations in relation to climate have been explored extensively on the southeastern Bering Sea shelf, specifically in relation to recruitment of the commercially important species walleye pollock (Gadus chalcogrammus). We addressed two research questions in this study: (i) Does the relative abundance of individual copepod species life history stages differ across warm and cold periods and (ii) Do estimated secondary production rates for copepods differ across warm and cold periods? For most copepod species, warmer conditions resulted in increased abundances in May, the opposite was observed in colder conditions. Abundances of smaller‐sized copepod species did not differ significantly between the warm and cold periods, whereas abundances of larger‐sized Calanus spp. increased during the cold period during July and September. Estimated secondary production rates in the warm period were highest in May for smaller‐sized copepods; production in the cold period was dominated by the larger‐sized Calanus spp. in July and September. We hypothesize that these observed patterns are a function of temperature‐driven changes in phenology combined with shifts in size‐based trophic relationships with primary producers. Based on this hypothesis, we present a conceptual model that builds upon the Oscillating Control Hypothesis to explain how variability in copepod production links to pollock variability. Specifically, fluctuations in spring sea‐ice drive regime‐dependent copepod production over the southeastern Bering Sea, but greatest impacts to upper trophic levels are driven by cascading July/September differences in copepod production.     

Ichthyophonus‐infected walleye pollock Theragra chalcogramma (Pallas) in the eastern Bering Sea: a potential reservoir of infections in the North Pacific

In 2003, the Alaska walleye pollock industry reported product quality issues attributed to an unspecified parasite in fish muscle. Using molecular and histological methods, we identified the parasite in Bering Sea pollock as Ichthyophonus. Infected pollock were identified throughout the study area, and prevalence was greater in adults than in juveniles. This study not only provides the first documented report of Ichthyophonus in any fish species captured in the Bering Sea, but also reveals that the parasite has been present in this region for nearly 20 years and is not a recent introduction. Sequence analysis of 18S rDNA from Ichthyophonus in pollock revealed that consensus sequences were identical to published parasite sequences from Pacific herring and Yukon River Chinook salmon. Results from this study suggest potential for Ichthyophonus exposures from infected pollock via two trophic pathways; feeding on whole fish as prey and scavenging on industry‐discharged offal. Considering the notable Ichthyophonus levels in pollock, the low host specificity of the parasite and the role of this host as a central prey item in the Bering Sea, pollock likely serve as a key Ichthyophonus reservoir for other susceptible hosts in the North Pacific.