Daily and sub-daily otolith increments of larval and juvenile walleye pollock, Theragra chalcogramma (Pallas), as validated by alizarin complexone experiments

Walleye pollock (Theragra chalcogramma) were reared from eggs to the juvenile life stage to study daily increment formation in the sagittae otoliths, which are routinely used for age and growth analyses. The apparent deposition of sub-daily growth increments becomes problematic for determining fish age from the late larval stage throughout the juvenile (young-of-the-year) development stage. Otolith marking experiments were conducted to determine interpretation criteria to differentiate between daily and sub-daily increments. Immersion of larval and transforming walleye pollock in 25 mg/l of alizarin complexone (ALC) for 6 h once a week produced a fluorescent mark on the day of staining. Evidence of six well defined and equally spaced increments counted between the weekly ALC marks validated the deposition of daily increments. The daily increments gradually increased in width as the fish/otolith grew. The criteria for determining the presence of sub-daily increments between the daily increments were (1) weak optical definition and (2) a sudden change in incremental distance that lasted for one or two increments and were approximately <0.5 μm in width. Growth problems that occurred during the experiments were identified on otoliths as reductions in daily incremental widths and optical definition, which continued for several days. Otoliths from field-collected fish have also shown similar changes in daily increment properties during the juvenile stage, which may be an indicator of an environmental influence. The criteria for defining different increment types help to resolve our current age determination issues for late larval and early juvenile stage walleye pollock from the Gulf of Alaska.     

Improved growth of flathead flounder Hippoglossoides dubius in hypoxic waters in Funka Bay,Japan

To identify the factors that influence the growth rate of flathead flounder Hippoglossoides dubius in Funka Bay, Japan, we studied temporal changes in the growth of this species and its prey from 1989 to 2012. The lowest growth rate of H. dubius was recorded in the 1995 year-class, which had experienced severe hypoxia between 1995 and 1997. However, the highest growth rate was recorded in the 2007 year-class, which had experienced hypoxia between 2009 and 2011. In 2000 and 2001, small-sized flounder (<200 mm TL) from the 1995 year-class were feeding on mysidaceans, whereas those from other year-classes fed on small Ophiura spp. (<9 mm in disc diameter) in 2009, 2011, and 2012. Small Ophiura spp. were more abundant in 2007 and 2011 than in 2002 and 2003. Successful recruitment of Ophiura spp. took place between 2007 and 2011 and cohorts from these years could tolerate hypoxia. This suggests that food availability improved under hypoxic conditions, which led to improved growth in small flounders. Large flounders (≥200 mm TL) from all year-classes fed on prickleback fishes (Stichaeidae) and walleye pollock Gadus chalcogrammus juveniles. The growth of large flounders was enhanced by an increase in the abundance of Stichaeidae fishes and G. chalcogrammus juveniles.     

Interannual variability in hatching period and early growth of juvenile walleye pollock, Theragra chalcogramma, in the Pacific coastal area of Hokkaido

Juvenile walleye pollock of the Japanese Pacific population were collected from the Funka Bay [spawning ground; 16–64 mm fork length (FL)] in spring and the Doto area (nursery ground; 70–146 mm FL) in summer. Hatch dates were estimated by subtracting the number of otolith daily increments from sampling dates, and their early growth was back‐calculated using otolith radius–somatic length relationships. Interannual change of the hatching period was observed during 2000–02, and the peaks ranged from mid‐February in 2000 to early‐April in 2002. In 2000, when a strong year class occurred, early life history of the surviving juveniles could be characterized by early hatching and slower growth in the larval stage (<22 mm length). Higher growth rate in 2001 and 2002 did not always lead to good survival and recruitment success. Even though their growth was slow in 2000, the larvae hatched early in the season had larger body size on a given date than faster‐growing larvae hatched in later season in 2001 and 2002. Bigger individuals at a certain moment may have advantage for survival. The delay of hatching period may result in higher size‐selective mortality, and as a necessary consequence, back‐calculated growth in 2001 and 2002 could shift towards higher growth rate, although abundance of such a year class would be at the lower level. Variability in spawning period, early growth and their interaction might have a strong relation to larval survival through cumulative predation pressure or ontogenetic changes in food availability.     

Variations in larval walleye pollock feeding and condition: a synthesis

There was a strong association among concentrations of microzooplankton prey sampled from the walleye pollock, Theragra chalcogramma , larval habitat, gut contents of larvae, and their nutritional condition. Subsequently, hypothesized survival potentials linked to food availability were validated by independently determined mortality rates. We present evidence that a significant number of walleye pollock larvae were starving in 1991 but that fewer were starving in 1992. At some stations where prey levels were anomalously low in 1991, up to 40% of the larvae were in poor condition. There appears to be a 2-week period after first feeding when walleye pollock are vulnerable to starvation.     

Simulation of physically mediated variability in prey resources of a larval fish: a three-dimensional NPZ model

A three-dimensional biophysical nutrient–phytoplankton–zooplankton model was used to investigate the spatial and temporal dynamics of food resources for young walleye pollock in the western Gulf of Alaska, to further understanding of recruitment processes for pollock. We modeled nitrogen, phytoplankton, a large herbivorous grazer parameterized as Neocalanus spp. (the biomass dominant copepod in the Gulf), and the 13 stages (egg, naupliar and copepodite) of Pseudocalanus spp. (a major constituent of the diet of pollock) so that the appropriate size class of food for each size of larval pollock was represented. Model results identified an area between the Semidi and Shumagin Islands that may not be suitable as a nursery area early in the year due to low prey abundance. Modeled mesoscale eddies, previously hypothesized to be important for larval pollock retention in Shelikof Strait, contained higher prey concentrations than the surrounding waters when they were cyclonic. This work also help to understand the consistency of pollock spawning in time and space in Shelikof Strait, by examining the timing and location of prey availability which, along with transport, narrows the window for optimal spawning.     

Changes in lipid classes,fatty acids,protein and amino acids during egg development and yolk‐sac larvae stage in brill (Scophthalmus rhombus L.)

Brill (Scophthalmus rhombus L.) is a flatfish considered of special interest for aquaculture diversification, but the high mortality observed during the early larval rearing is the main obstacle to commercial culture. The objective of this study was to contribute to the knowledge of nutrient utilization of early‐hatched larvae, characterizing the changes in lipid and protein contents during embryogenesis and the yolk‐sac larval stage of S. rhombus. Total lipid, lipid classes and fatty acid contents remained constant during embryogenesis and yolk‐sac larval development, except for phosphatidylethanolamine and phosphatidylinositol, which increased in quantity during the yolk‐sac larval stage. On the other hand, total protein (including non‐protein nitrogen) and amino acids decreased their contents in both periods, especially at hatching. The decrease only in the serine, glutamic acid, proline and lysine contents during embryogenesis suggests a selective use of amino acids during this phase. Unlike embryogenesis, amino acids loss during hatching appears to be non‐selective, and almost all amino acids (essential and non‐essential) decreased. Our results suggest that there is higher catabolism of protein vs. lipid during embryogenesis and the yolk‐sac larval stage of S. rhombus.     

Effect of environmental factors and prey species on daytime and nighttime vertical distribution of juvenile walleye pollock in and around Funka Bay

We examined factors affecting the vertical distribution of juvenile walleye pollock during “the second critical period” (i.e. the transition period of prey size) in and around Funka Bay, Hokkaido, Japan. During the day, small juveniles (<30 mm) were distributed mainly in shallow, warm, and low-salinity water within the bay, whereas larger ones (≥30 mm) occurred in deeper, cold and saline water. During the night, the large juveniles migrated to shallower depths. Outside the bay, small- and large-sized juveniles were distributed in water masses of similar physical properties during the daytime, whereas during the nighttime, most of the juveniles moved to shallower depth, and some juveniles dived to deeper water mass. Dietary analysis revealed that large juveniles fed on large copepods (≥0.5 mm in body width) more than small juveniles did. The composition of zooplankton in our survey area showed that large-sized copepods often occurred in deeper saline water. From these results, there is a possibility that juvenile pollock inside and outside Funka Bay occupied different water masses preferable for each feeding advantage.     

Utilization of free amino acids, yolk proteins and lipids in developing eggs and yolk-sac larvae of walleye pollock Theragra chalcogramma

ABSTRACT:   To elucidate the utilization of the major yolk nutrient stocks in eggs and larvae of walleye pollock Theragra chalcogramma , the contents of free amino acids (FAA), the major yolk protein (180 kDa lipovitellin originated from vitellogenin B in ovulated eggs: oLv B), and lipids were measured. Most eggs hatched 18 days after fertilization at 5°C, and all larvae absorbed almost all their yolk mass by 28 days. The total FAA content showed no change during the first 6 days, and then decreased to 28% of the initial level by 18 days. The oLv B contents, measured by an enzyme-linked immunosorbent assay using a specific antiserum against oLv B, gradually decreased from 6 to 18 days, followed by a rapid decline. The content of phospholipids (PL) and triacylglycerols (TG) showed no marked change until hatching, and then decreased until disappearance of yolk sac. From these results, it is proposed that there are two main periods for nutrient utilization in embryos and larvae of walleye pollock. In the first period, FAA was mainly utilized until 18 days after fertilization. Active utilization of oLv B and lipids (PL and TG) instead of FAA occurred during the second period from 18 to 28 days.     

Prey selection of common minke (Balaenoptera acutorostrata) and Bryde's (Balaenoptera edeni) whales in the western North Pacific in 2000 and 2001

A study of common minke and Bryde's whales was conducted in the western North Pacific in the 2000 and 2001 summer seasons to estimate prey selection of cetaceans as this is an important parameter in ecosystem models. Whale sighting and sampling surveys and prey surveys using quantitative echosounder and mid‐water trawl were carried out concurrently in the study. Biomasses of Japanese anchovy, walleye pollock and krill, which were major prey species of common minke and Bryde's whales, were estimated using an echosounder. The results suggested that common minke whale showed prey selection for Japanese anchovy while they seemed to avoid krill in both the offshore and coastal regions and walleye pollock in the continental shelf region. Selection for shoaling pelagic fish was similar to that in the eastern North Atlantic. Bryde's whale showed selection for Japanese anchovy in August 2000 and July 2001, while it showed prey selection for krill in May and June in 2001.     

Spatio‐temporal analyses of marine predator diets from data‐rich and data‐limited systems

Accounting for variation in prey mortality and predator metabolic potential arising from spatial variation in consumption is an important task in ecology and resource management. However, there is no statistical method for processing stomach content data that accounts for fine‐scale spatio‐temporal structure while expanding individual stomach samples to population‐level estimates of predation. Therefore, we developed an approach that fits a spatio‐temporal model to both prey‐biomass‐per‐predator‐biomass data (i.e. the ratio of prey biomass in stomachs to predator weight) and predator biomass survey data, to predict “predator‐expanded‐stomach‐contents” (PESCs). PESC estimates can be used to visualize either the annual landscape of PESCs (spatio‐temporal variation), or can be aggregated across space to calculate annual variation in diet proportions (variation among prey items and among years). We demonstrated our approach in two contrasting scenarios: a data‐rich situation involving eastern Bering Sea (EBS) large‐size walleye pollock (Gadus chalcogrammus, Gadidae) for 1992–2015; and a data‐limited situation involving West Florida Shelf red grouper (Epinephelus morio, Epinephelidae) for 2011–2015. Large walleye pollock PESC was predicted to be higher in very warm years on the Middle Shelf of the EBS, where food is abundant. Red grouper PESC was variable in north‐western Florida waters, presumably due to spatio‐temporal variation in harmful algal bloom severity. Our approach can be employed to parameterize or validate diverse ecosystem models, and can serve to address many fundamental ecological questions, such as providing an improved understanding of how climate‐driven changes in spatial overlap between predator and prey distributions might influence predation pressure.     

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.     

Coupling ecosystem and individual‐based models to simulate the influence of environmental variability on potential growth and survival of larval sprat (Sprattus sprattus L.) in the North Sea

To investigate the impact of changing environmental conditions in the North Sea on the distribution and survival of early life stages of a marine fish species, we employed a suite of coupled model components: (i) an Eulerian coupled hydrodynamic/ecosystem (Nutrients, Phyto‐, Zooplankton, Detritus) model to provide both 3‐D fields of hydrographical properties, and spatially and temporally variable prey fields; (ii) a Lagrangian transport model to simulate temporal changes in cohort distribution; and (iii) an individual‐based model (IBM) to depict foraging, growth and survival of fish early life stages. In this application, the IBM was parameterized for sprat (Sprattus sprattus L.) and included non‐feeding (egg and yolk‐sac larval) stages as well as foraging and growth subroutines for feeding (post‐yolk sac) larvae. Sensitivity analyses indicated that the angle of visual acuity, assimilation efficiency and the maximum food consumption rate were the most critical intrinsic model parameters. As an example, we applied this model system for 1990 in the North Sea. Results included not only information concerning the interplay of temperature and prey availability on larval fish survival and growth but also information on mechanisms underlying larval fish aggregation within frontal zones. The good agreement between modelled and in situ estimates of sprat distribution and growth rates in the German Bight suggested that interconnecting these different models provided an expedient tool to scrutinize basic processes in fish population dynamics.     

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.     

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 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.     

The influence of pelagic habitat selection and interspecific competition on productivity of juvenile walleye pollock (Theragra chalcogramma) and capelin (Mallotus villosus) in the Gulf of Alaska

Here we investigate processes affecting productivity of capelin and walleye pollock in the Gulf of Alaska. We examine pelagic habitat selection by comparing the distribution of juvenile fish and their prey with oceanographic properties and we evaluate the potential for interspecific competition by comparing diets and measures of foraging. The primary field study was conducted in Barnabus Trough, Kodiak Island, Alaska, during September 2005. The distribution of fish was assessed acoustically and trawls were used to collect individual fish for stomach content analyses. Physical and biological data were collected with conductivity–temperature–depth probes and zooplankton tows. Age‐0 pollock were distributed in cool waters offshore of a mid‐trough front, coincident with the distribution of euphausiids, their preferred prey. In contrast, capelin and their prey (copepods) were distributed throughout the trough. We observed that sympatric capelin (occurring with pollock) often had reduced foraging success compared to allopatric capelin (occurring alone). Results of a bioenergetic model also suggest that the exclusion of capelin from foraging on euphausiids can have negative consequences for capelin growth.     

Mortality of larval walleye pollock Theragra chalcogramma in the western Gulf of Alaska, 1988–91

Mortality rates of larval walleye pollock Theragra chakogramma were estimated from larval survey data from 1988 to 1991. Mortality estimates were based on cohort-specific losses between occupations of survey grids. Interannually, estimates of early feeding stage larval mortality rates ranged over an order of magnitude, from 0.045–0.43 day^-1, and declined sharply with age. There is some evidence that mortality rates of early feeding larvae tend to be negatively correlated with temperature and postively correlated with wind mixing.     

Predation on walleye pollock (Theragra chakograrnma) eggs and yolk-sac larvae by pelagic crustacean invertebrates in the western Gulf of Alaska

Immunological detection of yolk protein was used to assess predation by pelagic amphipods (gammarid and hyperiid), mysids, and euphausiids on eggs and yolk-sac larvae of walleye pollock Theragra chalcogramma during 1988 and 1989. Consumption estimates were made on the basis of frequency of positive immunoassays, assay detection times (gut clearance time), predator abundance, and spatial overlap of predators and prey. From our results gammarid amphipods and euphausiids were important predators on eggs and yolk-sac larvae, respectively. Gammarid amphipods alone consumed about 14% of the standing stock of pollock eggs in 1989. These results were compared with those from clearance rate experiments of predators feeding on pollock eggs in 300-1 bags. In general, clearance rate estimates of egg consumption were lower than those determined from gut contents.     

Mortality processes of hatchery‐reared Pacific bluefin tuna Thunnus orientalis (Temminck et Schlegel) larvae in relation to their piscivory

In mass culture of Pacific bluefin tuna Thunnus orientalis, yolk‐sac larvae of other species are fed as a major prey item to tuna larvae from 7 to 8 mm in total length. Marked growth variations in tuna larvae are frequently observed after feeding of yolk‐sac larvae, and this variation in the growth of tuna larvae is subsequently a factor leading to the prevalence of cannibalistic attacks. To elucidate details of the mortality process of hatchery‐reared tuna larvae after the initiation of yolk‐sac larvae feeding, we compared the nutritional and growth histories of the surviving (live) tuna larvae to those of the dead fish, found dead on the bottom of the tank, as direct evidence of their mortality processes. Cause of mortality of tuna larvae 3 and 5 days after the initiation of feeding of yolk‐sac larvae was assessed from nitrogen stable isotope and otolith microstructure analyses. Stable isotope analysis revealed that the live fish rapidly utilized prey fish larvae, but the dead fish had depended more on rotifers relative to the live fish 3 and 5 days after the initiation of feeding of yolk‐sac larvae. The growth histories based on otolith increments were compared between the live and dead tuna larvae and indicated that the live fish showed significantly faster growth histories than dead fish. Our results suggest that fast‐growing larvae at the onset of piscivory could survive in the mass culture tank of Pacific bluefin tuna and were characterized by growth‐selective mortality.