Climate change in the southeastern Bering Sea: impacts on pollock stocks and implications for the oscillating control hypothesis

Concern about impacts of climate change in the Bering Sea prompted several research programs to elucidate mechanistic links between climate and ecosystem responses. Following a detailed literature review, Hunt et al. (2011) (Deep‐Sea Res. II, 49, 2002, 5821) developed a conceptual framework, the Oscillating Control Hypothesis (OCH), linking climate‐related changes in physical oceanographic conditions to stock recruitment using walleye pollock (Theragra chalcogramma) as a model. The OCH conceptual model treats zooplankton as a single box, with reduced zooplankton production during cold conditions, producing bottom‐up control of apex predators and elevated zooplankton production during warm periods leading to top‐down control by apex predators. A recent warming trend followed by rapid cooling on the Bering Sea shelf permitted testing of the OCH. During warm years (2003–06), euphausiid and Calanus marshallae populations declined, post‐larval pollock diets shifted from a mixture of large zooplankton and small copepods to almost exclusively small copepods, and juvenile pollock dominated the diets of large predators. With cooling from 2006–09, populations of large zooplankton increased, post‐larval pollock consumed greater proportions of C. marshallae and other large zooplankton, and juvenile pollock virtually disappeared from the diets of large pollock and salmon. These shifts in energy flow were accompanied by large declines in pollock stocks attributed to poor recruitment between 2001 and 2005. Observations presented here indicate the need for revision of the OCH to account for shifts in energy flow through differing food‐web pathways due to warming and cooling on the southeastern Bering Sea shelf.     

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.     

Chum salmon (Oncorhynchus keta) growth and temperature indices as indicators of the year–class strength of age‐1 walleye pollock (Gadus chalcogrammus) in the eastern Bering Sea

Ecosystem‐based fisheries management requires the development of physical and biological time series that index ocean productivity for stock assessment and recruitment forecasts for commercially important species. As recruitment in marine fish is related to ocean condition, we developed proxies for ocean conditions based on sea surface temperature (SST) and biometric measurements of chum salmon (Oncorhynchus keta) captured in the walleye pollock (Gadus chalcogrammus) fishery in the eastern Bering Sea in three periods (July 16–30, September 1–15 and September 16–30). The main purpose of this paper was to evaluate Pacific salmon (Oncorhynchus spp.) growth as a possible indicator of ocean conditions that, in turn, may affect age‐1 walleye pollock recruitment. Marine growth rates of Pacific salmon are the result of a complex interplay of physical, biological and population‐based factors that fish experience as they range through oceanic habitats. These growth rates can, therefore, be viewed as indicators of recent ocean productivity. Thus, our hypothesis was that estimated intra‐annual growth in body weight of immature and maturing age‐4 male and female chum salmon may be used as a biological indicator of variations in rearing conditions also experienced by age‐0 walleye pollock; consequently, they may be used to predict the recruitment to age‐1 in walleye pollock. Summer SSTs and chum salmon growth at the end of July and September explained the largest amount of variability in walleye pollock recruitment indicating that physical and biological indices of ocean productivity can index fish recruitment.     

Multispecies biomass dynamics models reveal effects of ocean temperature on predation of juvenile pollock in the eastern Bering Sea

Walleye pollock (Gadus chalcogrammus) supports one of the largest commercial fisheries in the world. Juvenile pollock are important forage fish in the eastern Bering Sea (EBS) ecosystem, often representing the largest fraction in the diets of major Bering Sea piscivores. Large variability in the EBS pollock stock biomass in recent years has been attributed primarily to fluctuations in recruitment. It has been hypothesized that predation rates on forage fishes increase when the cold pool (a body of cold water < 2°C) is extensive and covers much of the middle continental shelf, which tends to concentrate larger predatory fishes in the outer shelf and slope regions. In contrast, young pollock appear to tolerate colder temperatures than older fish and can stay in the cold pool, thereby reducing predation. We used a multispecies modeling approach to examine the effects of the cold pool size on predation of juvenile pollock. We found that predation on age‐1 pollock by age‐3+ pollock decreased, and predation on age‐1 and age‐2 pollock by arrowtooth flounder increased with increasing bottom temperature, which was used as a proxy for the cold pool size. These results suggest that the cold pool creates spatial separation between juvenile pollock and arrowtooth flounder, but not between adult and juvenile pollock. The model developed in this study could be used to examine the effects of other covariates on interspecific interactions, help explain observed changes in fish communities, and understand implications of climate change on ecosystems and their productivity.     

A review: Walleye pollock in the North Pacific–how much difference do they really make?

Populations of several species of marine birds and mammals in the Bering Sea and Gulf of Alaska have been declining since the mid-1970s, with numbers of one, the Steller sea lion (Eumetopias jubatus) , so depressed it was listed as threatened under the Endangered Species Act in spring 1990. All of the declining populations depend to an important extent on walleye pollock (Theragra chakogramma) for food, although they eat numerous other species as well. In contrast, certain animals that compete with pollock for common prey have been increasing in abundance. All of these changes could be related through food web connections mediated by pollock. Pollock is also important to people–it presently supports the largest single-species commercial fishery in the world, in large part because of its great biomass, which has averaged about 15 × 10⁶t in the Bering Sea over the past 15 years. Pollock consume an inordinate proportion of the pelagic production in the Bering Sea, which further supports the conclusion that it is a key species in the ecosystem. However, there are conflicting hypotheses about the importance of the roles played by pollock as predator and prey, and about the effect that changes in pollock abundance might have on biomass yield at higher trophic levels.     

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.     

Interannual variability in growth of walleye pollock, Theragra chalcogramma, in the central Bering Sea

Interannual variability in growth of walleye pollock, Theragra chalcogramma, was examined. Adult walleye pollock were collected from the central Bering Sea (Aleutian Basin) from 1978 to 1999. Average fork lengths were found to be approximately 47 cm during the 1970–80s, this increased to 56 cm in the late 1990s. Age was determined for 4805 individuals using the otolith break and burn method. Ages ranged from 5–23 years and the year classes of 1978 and 1989 were dominant in the 1980s and the 1990s, respectively. Fish had significantly larger length-at-age in the 1990s compared to the 1970–80s, and interannual variability in age–length relationship was clearly observed. Taking into consideration a recent decrease of the walleye pollock biomass in the central Bering Sea, density-dependent growth was supported as one possibility of the growth variability. At the same time, we could not rule out the possibility that oceanographic variability affected the growth of walleye pollock in the area.     

Life-history traits of walleye pollock, Theragra chalcogramma, in the northeastern Japan Sea during early to mid 1990s

I examined the age, growth, maturity, mortality, and body condition of walleye pollock, Theragra chalcogramma, in the northeastern Japan Sea (northern Japan Sea population) and evaluated their resilience to exploitation. Walleye pollock were collected in pre-spawning (October 1991-1995) and post-spawning (April 1990-1996) seasons. Estimated ages ranged from 3 to 18 years for both sexes. A von Bertalanffy growth model showed that females had longer asymptotic fork length (460 mm) than males (425 mm). Fifty percent of females and males were mature at 348 mm (4.6 years) and 322 mm (3.9 years), respectively. The instantaneous natural mortality rate was estimated to be 0.22. These life-history traits in the northern Japan Sea population were compared to those in the Bering Sea, the Gulf of Alaska, and the Japan Pacific populations. As a result, female walleye pollock in this population matured at small body sizes, grew rapidly toward small maximum sizes, and had short reproductive lifespans with low size-specific fecundity and poor body condition. Low prey availability and habitat temperatures are considered as a possible mechanism for the small maximum sizes in this population. The potential rate of population increase of both the northern Japan Sea population and other pollock populations tended to be lower than other exploited populations of non-viviparous marine fishes, suggesting potentially lower resilience to exploitation in this population and walleye pollock populations in general.     

Effect of ocean conditions on the cross-shelf distribution of walleye pollock (Theragra chalcogramma) and capelin (Mallotus villosus)

Acoustic trawl surveys were conducted in 2000 and 2001 in two troughs located off the eastern coast of Kodiak Island in the Gulf of Alaska as part of a multiyear, multidisciplinary experiment to examine the influence of environmental conditions on the spatial distribution of adult and juvenile walleye pollock (Theragra chalcogramma) and capelin (Mallotus villosus). Continuous underway sea surface temperature samples and water column profiles collected in 2000 and 2001 showed the presence of a sharp shelf‐break front in Chiniak Trough and a mid‐trough front in Barnabas Trough. At distances <22 km from shore, the water column was well mixed, whereas a well‐defined mixed layer was present beyond approximately 22 km from shore. Satellite drifter tracks in Barnabas Trough entered along the upstream edge of the trough and appeared to follow the frontal boundary across the middle portion of the trough. A storm in 2001 weakened stratification and cooled surface water temperature by 1.6–2.1°C. Wind mixing associated with the storm event mixed subsurface chlorophyll a to the surface and enhanced nutrients in the surface waters. The storm event revealed spatial partitioning of summer production in Barnabas Trough, with production concentrated in regions inside the mid‐trough front. In contrast, post‐storm summer production was distributed throughout Chiniak Trough. The spatial distribution of walleye pollock and capelin differed and appeared to be related to differences in habitat characteristics. Acoustic survey data identified four acoustic sign types: age‐1 pollock, adult pollock, capelin, capelin–age‐0 pollock mix. The spatial distribution of these four sign types appears to be influenced by the oceanographic and topographic features of the two troughs. Adult pollock were broadly distributed throughout Chiniak Trough, whereas adult pollock were aggregated on the coastal side of the frontal system in Barnabas Trough. In 2000, capelin occurred with age‐0 pollock. In Chiniak Trough, capelin were most abundant along steep topographic gradients at the edges of the trough and in a deep region near Cape Chiniak, whereas the capelin–age‐0 mix (2000) or capelin (2001) concentrations were observed in slope water intrusions over the outer shelf in Barnabas Trough. Results suggest that habitat selection of walleye pollock and capelin are controlled by different processes. Capelin distributions appear to be limited by oceanographic conditions while other factors appear to be more important for pollock.     

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.