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.     

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.     

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.     

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.     

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.     

Eastern Bering Sea pollock recruitment,abundance, distribution and approach to fishery management

Eastern Bering Sea pollock have two distinctly different stable spawning grounds—along the shelf and in the eastern and central Aleutian Islands between 400 and 500 m water columns. Pollock spawning behavior supports the hypothesis that the shelf and deepwater “basin” spawning pollock are completely independent reproductive stocks. Deepwater pollock inhabit the shelf and, once mature at age 5–6 years, migrate from the shelf onto the continental slope into the Zhemchug, Pribilof, and Bering canyons by the end of winter. Bering Sea pollock recruitment and year class abundance have high annual variability, but there are no clear relationships between pollock year class strength and water temperature, ice distribution or survival on early ontogenesis stages (eggs and larvae). Young-of-the-year fish survival varies dramatically during winter supporting the hypothesis that the Bering Sea pollock recruitment and strength of year class have high annual variability depending on young-of-the-year fish survival during winter. The annual change of physical oceanography condition, productivity and species composition of zooplankton community are associated with great differences in pollock seasonal migrations and distribution, reproduction, survival of recruits at early stages of development and finally with abundance of year classes and total biomass. Implementation of ecosystem-based fishery management most important for application of pollock research both of Russian national program and on base of International Agreements.     

Walleye pollock: global overview

Walleye pollock is the second most extensively fished species in the world. The major fishing grounds include the Bering and Okhotsk Seas. Large-scale fishing started in the 1960s and continues to date with average annual landings over this 50-year period of 1.5 million tons. Yet over this period catches were characterized by considerable volatility. This volatility makes rational management of stock and planning of annual fishing activities difficult. The changes in annual catches correlate with the changes in the biomass of walleye pollock. Existing data suggest a close link between climate change in the northern Pacific and biomass, which allows quantitative estimates of future trends in the biomass, and consequently annual catch, of walleye pollock. Cooling of the northern Pacific is expected to increase the biomass in the Sea of Japan and decrease it in the Bering Sea and Sea of Okhotsk. The opposite is predicted to occur if the northern Pacific experiences warming.     

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.     

Interannual changes in the timing of walleye pollock spawning migration and their impacts on the gillnet fishery in the southwestern Pacific coast of Hokkaido,Donan area,Japan

The southwestern Pacific coast of Hokkaido is the main spawning ground for the Japanese Pacific stock of walleye pollock Theragra chalcogramma. A commercial gillnet fishery targeting spawning adult pollock in this area mainly operates from October to January to coincide with the migration of adult pollock from the feeding ground. Given the results of acoustic surveys, and changes in the proportion of the monthly total catch that was monthly walleye pollock caught by the commercial gillnet fishery, it is thought that the timing of walleye pollock spawning migration to the Donan area varies among years and that the pollock catch of the gillnet fishery clearly reflects changes in pollock abundance in this area. A time series of interannual variability in catch data from 1980 to 2005 suggested that adult pollock migrated and concentrated on their spawning ground later in the 1980s and after 2000 than in the 1990s. Such decadal-scale shifts are presumably caused by climatic changes (e.g., in water temperature) in the Oyashio region. These shifts affect the gillnet fishery through differences in monthly unit prices of pollock and changes in the formation of fishing grounds. These scientific findings can aid the establishment of rules for more efficient walleye pollock resource management under the total allowable catch system.     

Complete nucleotide sequence and variation of mitochondrial DNA from 10 individuals of walleye pollock, Theragra chalcogramma

ABSTRACT:   The complete mitochondrial genome sequence of 10 walleye pollocks, Theragra chalcogramma , from the Japan Sea and Bering Sea was determined. The 16 568–16 571 bp genome contains the same 37 mitochondrial structural genes (two ribosomal RNA, 22 transfer RNA, and 13 protein-coding genes) as found in all other vertebrates analyzed, in an organization identical to that of other bony fish. The major non-coding region had several conserved sequence features. Nucleotide variations of ND1, ND5, and control region were high, and these regions appear to be good candidates for high-resolution markers in population studies.     

Integrating seabird dietary and groundfish stock assessment data: Can puffins predict pollock spawning stock biomass in the North Pacific?

Information on the annual variability in abundance and growth of juvenile groundfish can be useful for predicting fisheries stocks, but is often poorly known owing to difficulties in sampling fish in their first year of life. In the Western Gulf of Alaska (WGoA) and Eastern Bering Sea (EBS) ecosystems, three species of puffin (tufted and horned puffin, Fratercula cirrhata, Fratercula corniculata, and rhinoceros auklet, Cerorhinca monocerata, Alcidae), regularly prey upon (i.e., “sample”) age-0 groundfish, including walleye pollock (Gadus chalcogramma, Gadidae) and Pacific cod (Gadus microcephalus, Gadidae). Here, we test the hypothesis that integrating puffin dietary data with walleye pollock stock assessment data provides information useful for fisheries management, including indices of interannual variation in age-0 abundance and growth. To test this hypothesis, we conducted cross-correlation and regression analyses of puffin-based indices and spawning stock biomass (SSB) for the WGoA and EBS walleye pollock stocks. For the WGoA, SSB leads the abundance of age-0 fish in the puffin diet, indicating that puffins sample the downstream production of the WGoA spawning stock. By contrast, the abundance and growth of age-0 fish sampled by puffins lead SSB for the EBS stock by 1–3 years, indicating that the puffin diet proxies incoming year class strength for this stock. Our study indicates connectivity between the WGoA and EBS walleye pollock stocks. Integration of non-traditional data sources, such as seabird diet data, with stock assessment data appears useful to inform information gaps important for managing US fisheries in the North Pacific.     

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.     

Interannual–interdecadal variations in zooplankton biomass, chlorophyll concentration and physical environment in the subarctic Pacific and Bering Sea

Interannual, decadal and interdecadal variations in summer plankton biomass during 1954–1994 in the whole subarctic Pacific and Bering Sea were compared among regions as well as with climatic and oceanographic conditions. The zooplankton biomass and chlorophyll concentration during the mid 1960s to early 1970s in the central and western subarctic Pacific were a few times higher than those in the preceding and following decades. The values in the eastern Bering Sea and eastern subarctic Pacific also increased in the mid 1960s, but remained at an elevated level until the end of the 1980s. These decades of higher and mid plankton biomass levels during the mid 1960s to early 1970s and mid 1970s to late 1980s correspond to the period of positive and negative values of the Northern Hemisphere zonal index (NHZI), respectively. In the decadal scale, one can see a significant positive correlation between the summer plankton biomass and the wind speed during winters in the eastern Bering Sea. The effect of grazing by biennially fluctuating Asian pink salmon on zooplankton biomass and its effect on chlorophyll concentration in the central subarctic Pacific is also significant.     

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.     

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.     

Mass-processing method for aging otoliths of walleye pollock <Emphasis Type="Italic">Theragra chalcogramma</Emphasis> using black resin

ABSTRACT:   The reliability of a mass-processing aging method for walleye pollock Theragra chalcogramma was examined. The method is a half-otolith method, in which 10–20 otoliths are embedded simultaneously in black resin and the mass-processed half plane section is viewed under reflected light (black-resin method). Seasonal periodicity of otolith growth was confirmed by the monthly observations of the percent of translucent zone at the otolith edge, and interannual variation in age distribution detected the progression of dominant year-classes. These results support the assumption that the translucent zone is formed once a year. The black-resin method was compared to the break–burn method, which is the standard technique for this species. The estimated ages of these methods were not biased throughout the age range examined. The coefficient of variation in the black-resin method (4.9–5.7%) was similar to those of the break–burn method (3.5–5.5%). These results suggest that the black-resin method is reliable as an aging method for walleye pollock.     

Proximate composition of some north-eastern Pacific forage fish species

To understand the relative dietary value of forage fish as prey in the Bering Sea and Gulf of Alaska, whole organisms of 13 species were analysed for proximate composition (protein, oil, ash and moisture content). Eulachon ( Thaleichthys pacificus ) were high in oil (total lipid) (16.8% to 21.4%) and low in moisture (64.6% to 70.8%). Oil in capelin ( Mallotus villosus ) ranged from 2.1% to 14.0%. Juveniles of walleye pollock ( Theragra chalcogramma ), Atka mackerel ( Pleurogrammus monopterygius ), Pacific herring ( Clupea pallasii ), and prowfish ( Zaprora silenus ) had low oil contents (< 1.8%) and high moisture contents (> 80.3%). Rankings of median proximate values illustrate the similarities. Surf smelt ( Hypomesus pretiosus ), rainbow smelt ( Osmerus mordax ), pricklebacks ( Lumpenus spp.), Atka mackerel, Pacific sand lance ( Ammodytes hexapterus ) and Pacific sandfish ( Trichodon trichodon ) ranked high in median protein content (> 15.4%). Median ash content for all species ranged from 0.6% to 3.3%. Total wet mass caloric content (kcal g^–1) was calculated for the four main species and a linear model was developed for caloric content as a function of moisture. The linear models (caloric content = b₀ + b₁ × moisture) were Pacific sand lance and Pacific sandfish (b₀ = 7.82, b₁ = – 0.09); eulachon (b₀ = 7.97, b₁ = – 0.08); and capelin (b₀ = 9.70, b₁ = – 0.11).     

Spatial and temporal patterns of walleye pollock (Theragra chalcogramma) spawning in the eastern Bering Sea inferred from egg and larval distributions

Walleye pollock Theragra chalcogramma (pollock hereafter) is a key ecological and economic species in the eastern Bering Sea, yet detailed synthesis of the spatial and temporal patterns of pollock ichthyoplankton in this important region is lacking. This knowledge gap is particularly severe considering that egg and larval distribution are essential to reconstructing spawning locations and early life stages drift pathways. We used 19 yr of ichthyoplankton collections to determine the spatial and temporal patterns of egg and larval distribution. Generalized additive models (GAMs) identified two primary temporal pulses of pollock eggs, the first occurring from 20 February to 31 March and the second from 20 April to 20 May; larvae showed similar, but slightly lagged, pulses. Based on generalized cross‐validation and information theory, a GAM model that allowed for different seasonal patterns in egg density within three unique areas outperformed a GAM that assumed a single fixed seasonal pattern across the entire eastern Bering Sea. This ‘area‐dependent’ GAM predicted the highest densities of eggs (i.e., potential spawning locations) in three major areas of the eastern Bering Sea: near Bogoslof Island (February–April), north of Unimak Island and the Alaska Peninsula (March–April), and around the Pribilof Islands (April–August). Unique temporal patterns of egg density were observed for each area, suggesting that pollock spawning may be more spatially and temporally complex than previously assumed. Moreover, this work provides a valuable baseline of pollock spawning to which future changes, such as those resulting from climate variability, may be compared.     

Tumours and microbial diseases of marine fishes in Alaskan waters

Abstract. In an effort further to define the current health status of demersal fish in the Bering Sea, 36 618 fish captured by otter trawl during 1976 were examined for pathological conditions. Of the 26 species examined, 22 were found to have no detectable abnormalities. The four species with abnormalities were Pacific cod Gadus macrocephalus Tilesius with pseudobranchial tumours and skin lesions, walleye pollock Theragra chalcogramma (Pallas) with pseudobranchial tumours, yellowfin sole Limanda aspera (Pallas) with lymphocystis, and rock sole Lepidopsetta bilineata (Ayres) with epidermal papillomas. The prevalence, geographical distribution and biological and pathological characteristics of affected individuals were determined.
Pseudobranchial tumours of both Pacific cod and walleye pollock were occasionally found to be invasive. Fish bearing these tumours were distributed throughout the sampling area. The epidermal papillomas on rock sole resembled similar tumours found on several flatfish species along the West Coast of North America. The distribution of this disease appeared to be depth related. The virus-caused lymphocystis growths were located on the 'blind' side of yellowfin sole. The highest frequencies of fish with lymphocystis were in the south-eastern Bering Sea. Two main types of skin lesions were seen on Pacific cod: ulcers and ring-shaped lesions. Isolates of bacteria ( Pseudomonas sp.) were routinely obtained from the cod ulcers and may be the cause of this disease. The ring-shaped skin lesions, when examined microscopically, contained unidentified epidermal basophilic bodies.     

The food habits of four species of triakid sharks, Triakis scyllium, Hemitriakis japanica, Mustelus griseus and Mustelus manazo, in the central Seto Inland Sea, Japan

ABSTRACT:   The food habits of 595 houndsharks of four species, Triakis scyllium ( n  = 179, 42–148 cm total in length), Hemitriakis japanica ( n  = 57, 42–102 cm), Mustelus griseus ( n  = 193, 39–100 cm), and Mustelus manazo ( n  = 166, 43–120 cm), found in the central Seto Inland Sea, Japan, from March 1997 to October 1999 and May 2000 to July 2002, were studied. T. scyllium changed their main food items from shrimps to echiuran worms then to cephalopods with their growth. Comparing food habits by the value of similarity (maximum = 1), the small-sized T. scyllium had a low value (0.17) compared to larger sharks. T. scyllium gradually increased the diversity of food until it reached 700 mm long in total length, however, after that it decreased. H. japanica appeared mainly in summer and autumn and ate cephalopods and fishes. M. griseus preyed on various crustaceans and decreased the diversity of food with growth. M. manazo preferred crustaceans and polychaetes. There was no certain tendency in the diversity of the food habit for M. manazo .