NOAA ERL Special Report

Bering Sea FOCI Final Report

S. Allen Macklin (editor)

Pacific Marine Environmental Laboratory

7600 Sand Point Way NE

Seattle, WA 98115

December 1998

Contribution 1964 from NOAA/Pacific Marine Environmental Laboratory

Contribution B356 from Fisheries-Oceanography Coordinated Investigations
NOTICE

Mention of a commercial company or product does not constitute an endorsement by

NOAA/ERL. Use of information from this publication concerning proprietary products or the

tests of such products for publicity or advertising purposes is not authorized.

Contribution No. 1964 from NOAA/Pacific Marine Environmental Laboratory

Contribution B356 from Fisheries-Oceanography Coordinated Investigations

For sale by the National Technical Information Service, 5285 Port Royal Road

Springfield, VA 22161

ii
Contents iii

Contents

Part 1—Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . 1

Part 2—Population ecology and structural dynamics of walleye

pollock, Theragra chalcogramma (Kevin M. Bailey) . . . . . . 3

Executive Summary . . . . . . . . . . . . . . . . . . . . . . . 3

2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2.2 Theoretical Framework: Structural Dynamics . . . . . . . . . 7

2.2.1 Distribution and Macroecology . . . . . . . . . . . . 7

2.2.2 Metapopulations and Geographical Structure . . . . 8

2.2.3 Genetic Structure . . . . . . . . . . . . . . . . . . . 10

2.3 Characterization of Pollock . . . . . . . . . . . . . . . . . . . 12

2.3.1 Distribution and Population Ecology . . . . . . . . 12

2.3.2 Year Class Dynamics . . . . . . . . . . . . . . . . . 17

2.4 Population Structuring Mechanisms in Pollock . . . . . . . . 17

2.4.1 Regional Oceanography and Transport . . . . . . . 20

2.4.2 Larval Transport, Eddy Retention, and Mortality . 21

2.4.3 Migration Patterns and Philopatry . . . . . . . . . . 28

2.4.4 Genetic and Metapopulation Structure . . . . . . . 35

2.4.5 Discussion of Gene Flow and Larval Transport . . . 42

2.4.6 Metapopulation Summary . . . . . . . . . . . . . . 43

2.5 Management Implications . . . . . . . . . . . . . . . . . . . . 45

2.6 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . 48

2.7 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48

Part 2A—The use of molecular techniques to dissect the genetic

architecture of pollock populations (Dennis A. Powers) . . 55

Part 2B—Trends in north Pacific pollock and 1998 harvest prognosis (Vidar G. Wespestad) . . . . . . . . . . . . . . . . . . . 65

Pollock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65

North American Pollock . . . . . . . . . . . . . . . . 65

Asian Pollock . . . . . . . . . . . . . . . . . . . . . . 68

Prognosis Summary fir 1998. . . . . . . . . . . . . 70

Part 3—Biophysical processes relevant to recruitment dynamics of walleye pollock (Theragra chalcogramma) in the Eastern

Bering Sea (J.M. Napp, A.W. Kendall, Jr., and J.D. Schumacher) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71

3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 71

3.1.1 Description of the Area . . . . . . . . . . . . . . . . 71

3.1.2 Description of the Problem . . . . . . . . . . . . . . 73

3.2 Physical Oceanographic Setting . . . . . . . . . . . . . . . . . 77

3.2.1 Marine Climatology and Sea Ice . . . . . . . . . . . 77

3.2.2 Oceanic Circulation . . . . . . . . . . . . . . . . . . 79

3.2.3 Eddies . . . . . . . . . . . . . . . . . . . . . . . . . 8 0

3.2.4 Exchange Between the Oceanic and Shelf

Regimes . . . . . . . . . . . . . . . . . . . . . . . . . 8 1

3.3 Production of Prey for Larval Pollock—Variability in the Timing and Magnitude of the Spring Phytoplankton Bloom . . . 84

3.3.1 Oceanic Regime . . . . . . . . . . . . . . . . . . . . 8 4

3.3.2 Shelf Regime . . . . . . . . . . . . . . . . . . . . . . 8 6

3.4 Larval Pollock Feeding . . . . . . . . . . . . . . . . . . . . . . 8 9
iv Contents

3.4.1 Oceanic Regime . . . . . . . . . . . . . . . . . . . . 8 9

3.4.2 Shelf Regime . . . . . . . . . . . . . . . . . . . . . . 91

3.5 Implications: Shelf and Oceanic Regimes as Feeding Environments for Pollock Larvae . . . . . . . . . . . . . . . . . . . . 94

3.5.1 Timing of Prey Production . . . . . . . . . . . . . . 94

3.5.2 Amount of Prey Produced . . . . . . . . . . . . . . 95

3.5.3 Taxonomic Composition of Prey . . . . . . . . . . . 95

3.5.4 Larval Condition . . . . . . . . . . . . . . . . . . . . 96

3.6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96

3.7 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . 98

3.8 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98

Part 3A—Juvenile pollock studies (R.D. Brodeur) . . . . . . . . 103

Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

Summer Distribution of Age-0 Pollock on the Eastern Bering

Sea Shelf . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

Distribution and Species Associations of Juvenile Pollock and

Forage Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . 105

Habitat Characteristics of Juvenile Pollock in the Eastern

Bering Sea . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105

Distribution of Juvenile Pollock and Other Biota in Relation

to Fronts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108

Commensal Associations of Juvenile Pollock with Schyphomedusae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108

Variability in Feeding and Condition of Age-0 Pollock in Relation to Fronts . . . . . . . . . . . . . . . . . . . . . . . . . . 112

Age and Growth of Juvenile Pollock in Relation to the Fronts 112

Covariation of Plankton, Juvenile Fish, and Seabirds at Tidal

Fronts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

Predation on Juvenile Pollock by Major Teleost Predators . . 115

Seabird Distributions Relative to Frontal Regions . . . . . . . 118

Fur Seal Distributions Relative to Frontal Regions . . . . . . 120

Part 3B—Modeling the upper ocean production dynamics of

plankton and larval pollock in the Bering Sea (Stephen M.

Bollens and Bruce W. Frost) . . . . . . . . . . . . . . . . . . 123

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124

Model Construction and Elaboration . . . . . . . . 124

Model Results-Generic Seasonal Cycles . . . . . . . 127

Multi-Species Model and Assimilation of 1992–1994

Physical Oceanographic Data . . . . . . . . . . . . . 128

Future Activities and Anticipated Milestones . . . . 133

Management Implications . . . . . . . . . . . . . . . . . . . . 133

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133

Part 3C—Seasonal sea ice in the Eastern Bering Sea (James D.

Schumacher and Tina Wyllie-Echeverria) ........... 135

Part 4—Administration and management of the Bering Sea FOCI

Program (S. Allen Macklin) . . . . . . . . . . . . . . . . . . . 139

4.1 Beginning of the Project . . . . . . . . . . . . . . . . . . . . . 139

4.2 Project Management . . . . . . . . . . . . . . . . . . . . . . . 141

4.3 Budget . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142

4.4 Competitive Process and Research Cycles . . . . . . . . . . . 142

4.5 Meetings and Workshops . . . . . . . . . . . . . . . . . . . . 143

4.6 Field Experiments . . . . . . . . . . . . . . . . . . . . . . . . 143
Contents v

4.7 Data Dissemination . . . . . . . . . . . . . . . . . . . . . . . 146

4.8 Project Reviews . . . . . . . . . . . . . . . . . . . . . . . . . 146

4.9 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146

Part 5—Selected monitoring, modeling, and technical achievements (compiled by S. Allen Macklin) . . . . . . . . . . . . 149

5.1 Monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149

5.2 Modeling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150

5.3 Technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151

5.4 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160

Part 6—Bering Sea FOCI Publication List . . . . . . . . . . . . . 163
vi Contents
Bering Sea FOCI Final Report

S. Allen Macklin (editor)

Part 1

Introduction

To develop an understanding of stock structure and recruitment variation

in Bering Sea pollock, the Coastal Ocean Program of the National Oceanic

and Atmospheric Administration (NOAA) funded an 7-year (1991–1997),

interdisciplinary project named Bering Sea Fisheries-Oceanography Coordinated Investigations (BS FOCI; Schumacher and Kendall, 1995) for which

NOAA and academic researchers were selected through a competitive process (Macklin, this report). The project goals, based on recommendations

from an international symposium on pollock (Aron and Balsiger, 1989) were

to (1) determine stock structure in the Bering Sea and its potential relationship to physical oceanography, and (2) examine recruitment processes in the

eastern Bering Sea. Both of these have direct implication to management.

An integrated set of field, laboratory, and modeling studies were established

to accomplish these goals. To address the first goal, project objectives were

to establish details of oceanic circulation relevant to larval dispersal and

separation of stocks, and determine if unique chemical or genetic indicators existed for different stocks. The recruitment component of BS FOCI,

addressing the second goal, focused on understanding causes of variable mortality of pollock larvae in the different habitats of the eastern Bering Sea.

The emphasis of recruitment studies was to determine the dominant physical oceanographic features (turbulence, temperature, and transport) that

could influence survival of pollock larvae, and investigate factors controlling

food production for the larvae. A later component contrasted juvenile habitat in three hydrographic regimes around the Pribilof Islands (Brodeur, this

report).

BS FOCI field studies included 20 cruises to the area, deployment of

four long-term biophysical moorings (some of which supported meteorological sensors), use of over 40 satellite-tracked drifters, and a series of aircraft

overflights (NOAA P3) using meteorological and ocean surface color and

temperature sensors (Macklin, this report). Laboratory studies examined genetic relationships, chemical composition of otoliths, assays of pollock larval

condition, and pollock larval feeding mechanisms and patterns. Modeling activities included basin circulation, one-dimensional nutrient-phytoplanktonzooplankton-fish relationships, and ecosystem aggregations.

This report comprises six parts. Part 1 is this Introduction. Part 2 discusses BS FOCI’s first goal, stock structure, and part 3 addresses BS FOCI’s

second goal, recruitment studies. Parts 4 and 5 present administration and

management of the project, and technical achievements, respectively. A list
2 S.A. Macklin (ed.)

of BS FOCI publications, numbering about 70 at the time this report was

written, is part 6 of this report.
Bering Sea FOCI Final Report 3

Part 2

Population ecology and structural dynamics of

walleye pollock, Theragra chalcogramma (Kevin M.

Bailey1)

Executive Summary

New paradigms for managing fisheries in a sustainable manner are under development; these renovated concepts will include better definitions of stock

distributions, interrelationships, and conservation. Management of many

marine fisheries has been based on the assumption of shallow (little) population structure with considerable gene flow. However, recent studies of

several species (previously assumed to be panmictic) using high resolution

techniques indicate more genetic structure than was found previously. These

results have implications for effective management, as overfishing of local

stocks can deplete the productivity of the larger (meta) population. A

summary view of genetic structure in walleye pollock suggests a pattern

of considerable geographic stock structure. Phenotypic differences between

stocks, elemental composition of otoliths, and parasite studies indicate restricted mixing of juveniles and adults. Genetic differences appear between

broad regions, but resolution between adjacent stocks, especially within the

eastern Bering Sea, is currently lacking. Genetic studies to date indicate

a varying degree of genetic differentiation between pollock in the Gulf of

Alaska and Bering Sea. The potential for gene flow during larval drift is

high between adjacent stocks, but since there appears to be an unresolved

degree of structuring within the Bering Sea, reduced gene flow due to larval retention mechanisms or strong natal homing and philopatry is possible.

Significant progress has been made in understanding the genetic structure

of pollock.

2.1 Introduction

Walleye pollock is among the world’s largest commercial fisheries with annual harvests ranging from 4 to 7 million tons in the North Pacific Ocean

over the past decade. In U.S. waters catches are on the order of 1.5 million

metric tons with a dollar value exceeding hundreds of millions. A large portion of the resource is bound for the export market, contributing to reduction

of the U.S. trade deficit. Without question, this natural resource is of critical importance to the health of domestic fisheries. Pollock is the dominant

groundfish species in many of the regional ecosystems across the North Pacific Ocean, including the eastern Bering Sea, and has been implicated in the

dynamics of higher trophic levels (see National Research Council, 1996). As

a key element in the North Pacific ecosystem, pollock is the target species for

numerous research programs, past and present, in the eastern Bering Sea as

well as in other seas. The stock structure of pollock is important knowledge

1Alaska Fisheries Science Center, NOAA, Seattle, WA 98115, U.S.A.
4 S.A. Macklin (ed.)

for management of this resource because of the potential for overfishing of

local stocks when it is assumed that large basin populations are panmictic.

The stock structure of pollock across the North Pacific Ocean, and especially in the Bering Sea, has been a topic of investigation for many years.

Many early studies were based on pollock’s phenotypic characteristics, such

as meristics and morphometrics, and other studies have been based on genotypic characters, such as DNA analyses. In general, biochemical genetic

studies have weakly distinguished eastern Pacific populations from western

Pacific populations, but phenotypic characters suggest a more detailed stock

structure. Only recently, using high resolution molecular techniques (Powers,

unpublished data: reported here) has there been good resolution between

populations on either side of the Bering Sea and between Gulf of Alaska

populations and eastern Bering Sea populations.

Fisheries resource management is based on the concept of renewable

stocks. For walleye pollock the regional stocks are managed separately; for

example, the Gulf of Alaska population is managed separately from the

Bering Sea, and the eastern and western Bering Sea and Aleutian Basin

populations are managed separately. However, there may be isolated populations on even finer scales; within the Gulf of Alaska there may be separate

spawning populations in Shelikof Strait, Prince William Sound, and the Shumagin Islands region. Furthermore, the degree of intermingling of stocks,

recolonization of depleted areas from healthy stocks, and other ecological

questions about resource mixing within the greater population framework

are almost completely unknown.

Although the overall catch of pollock on the U.S. side of the North Pacific

Ocean is relatively stable, some populations have experienced declines and

fisheries closures in recent years, including stocks in Puget Sound, Shelikof

Strait, Donut Hole, and Bogoslof Island. More recently, there are reports

that the western Pacific stocks are in a state of decline. Although eastern

Bering Sea shelf populations have been at healthy levels in the past, there

is concern about the sustainability of present harvest levels.

Pollock harvests were especially high from the mid-1980’s through about

1992 resulting from relatively strong recruitment, high abundance levels, and

unrestricted high seas fisheries. Wespestad (1996) lists 12 geographically

distinct stock (although not necessarily genetically distinct) groupings and

their catch trends (Table 2.1). Biomass and catch trends for the major

stock groupings indicate generally declining levels since the late-1980s in the

major fishing grounds (Figs. 2.1a, b). The greatest declines in biomass and

catches for pollock have been away from the center of pollock’s biomass.

For example, in the Gulf of Alaska, catches peaked at 307,000 tons in 1984

and have declined to 55,000 tons in 1996. At the extreme southern end

of its range in the eastern North Pacific, pollock in southern Puget Sound

may almost be extinct (Palsson et al., 1996). Likewise for the southern end

of its range in the western North Pacific around northern Japan, catches

are reduced by 3 to 4 times from their maximal values in the 1970’s (H.

Yoshida, Hokkaido Central Fisheries Experimental Station, Hamanaka 238,

Yoichi-cho, Hokkaido 046, Japan, personal communication, February 1994).

There are many complex and unresolved issues involving the structure of
Bering Sea FOCI Final Report 5

Figure 2.1: Trends in major stock grouping of walleye pollock: (a) Abundance trends for major stocks, (b)

catch trends for Asian and North American stocks (from Wespestad, 1996).
6 S.A. Macklin (ed.)

Table 2.1: Geographical distribution of walleye pollock stocks according to Wespestad (1996).

Stock Stock characteristics

North American

Southeast Alaska-Canada Small stock—minor fisheries

Western-Central Gulf of Alaska Variable stock, 50,000–200,000 t catch

Eastern Bering Sea Large stock, 1–2 million t catch

Asian

Northwest Bering Sea Mix of U.S. and Russian fish, 0.5–1 million t catch

Western Bering Sea Moderate stock, 0.5–1 million t catch

East Kamchatka Small-medium stock, 100,000–300,000 t catch

West Kamchatka Large stock, near 1 million t catch

North Sea of Okhotsk Moderate stock, 0.5–1 million t catch

Sakhalin Small stock, 65,000 t average catch

Kuril Islands Small-moderate stock

Japan Sea Heavily fished

Japan Pacific Moderate catch to 0.5 million t

the pollock population, including recent stock declines, discoveries of heretofore unknown stocks, potential consequences of fishing on certain elements

of the population, possible relationships between subunits, and potential

fishing pressure on the same subpopulation at different times from different geographic and quota regions. What is needed, but currently lacking,

is an understanding of the macroscale population ecology of pollock that

incorporates the relationship among different subpopulations of the greater

metapopulation, the rate of gene flow between these subpopulations, the

relationship between juvenile and adult distributions as linked together by

ontogenetic migrations, and the magnitude of colonization processes. A theoretical framework about the geographical structure and population ecology

of pollock needs to include recently developed ecological concepts that can

help us better understand the dynamics of this species and consider new

approaches to management. One such concept is macroecology, the study

of patterns of distribution of organisms in relation to their environment

(Brown, 1995). Many of the macroecological questions regarding pollock

are unanswered, such as the relationship between range size and population

abundance, and the effect of environmental factors on distribution of pollock. Another recent concept is that of metapopulation dynamics, the study

of conditions by which the processes of population turnover and establishment of new populations are maintained in balance (Hanski and Gilpin,

1991). Viewing pollock in the context of a metapopulation is a framework

to study the linkage of stock structure, dispersal, and colonization events.

In this report, the concepts of macroecology, metapopulations, and stock

structure are reviewed and areas where they intersect are indicated. Historical and current information on pollock, including mechanisms that may

isolate and maintain stock structure, are summarized and a “strawman”
Bering Sea FOCI Final Report 7

conceptual model of the population macroecology of walleye pollock is proposed.

2.2 Theoretical Framework: Structural Dynamics

The size of fish populations is determined by three major elements: (1)

available habitat determines the potential size, (2) dynamics within local

populations as influenced by the environment, competition, and predation

determine the specific size of a subpopulation, and (3) movement and colonization determine the spread of a population and modify local dynamics.

In this model, distribution, dispersal, and population structure are closely

linked, interwoven characteristics of metapopulations.

A population is a group of individuals of the same species living within a

sufficiently restricted area such that any member can mate with any other;

in large widespread populations it is recognized that individuals in the same

locality are more likely to mate and share common ancestry. Thus local

subpopulations can be made of largely intrabreeding units of geographically

structured populations. Geographical structure in populations is the nonrandom pattern of spatial distribution that may be related to historical or

current barriers between local populations, environmental patchiness, and/or

environmental gradients. The term structural dynamics integrates change

in population structure, and aspects thereof, such as range, genetics, and

dispersal patterns.

2.2.1 Distribution and Macroecology

Geographic range considerations are an important characteristic of populations. Species with broad niches become both widespread and locally abundant (Brown, 1984), and large ranges, abundance, and invasion ability are

linked characteristics within a species (Lawton et al., 1994). Species with extraordinary invasion abilities are generally those best adapted for marginal

habitats (MacArthur and Wilson, 1967). As described below, these concepts are especially relevant to pollock population biology. On the other

hand, specialized feeders, such as benthic feeding flatfishes, would appear to

be tied to specific habitat requirements; thus they cannot move and colonize new habitats freely as adults or settled juveniles compared with species

that have more generalized requirements. Furthermore, where the range of a

species with specialized requirements is made of a mosaic of habitat patches,

colonization by demersal stages may be impeded by regions of unfavorable

habitat.

Some populations may expand their range as they become more abundant, although others do not show this trend but show increases in local

density. As noted above, species with highly specialized niches may not

expand readily, and indeed no range/abundance relationships have been

found for some specialized flatfish species such as rock sole, Alaska plaice

(McConnaughey, 1995), and American plaice (Swain and Morin, 1996).

Thus for these species, the range size/population size relationship due to

density-dependent dispersal may not occur. More generalized species such
8 S.A. Macklin (ed.)

as Atlantic cod (Swain and Wade, 1993) and arrowtooth flounder (McConnaughey, 1995) expand their range as abundance increases.

Range expansions may be limited by physical impediments, such as temperature, salinity, and substrate availability, and by biological factors, including the presence of competitors and predators. There is also historical

structure in the environment, such as changes in the occupation of niches

due to disease and environmental events. Often when competition or predation pressure is removed there is an “ecological release” (MacArthur and

Wilson, 1967), resulting in an invasion event.

2.2.2 Metapopulations and Geographical Structure

Within the distributional range of animals, there may be considerable structure. The realization that animal populations are composed of local populations has a rich history going back to Andrewartha and Birch (1954).

In fisheries, knowledge of local populations goes back to the developments

and ideas of Schmidt, Heincke, and Hjort in the early 1900s (Sinclair, 1988).

The concept of population structure was formalized as that of metapopulations by Levins (1970). In the metapopulation view, a local population is

the spatial unit within which most interaction such as breeding occurs, and

a metapopulation is an ensemble of local populations (Taylor, 1991a) with

some potential of interaction.

Harrison (1991) showed five potential types of metapopulations with examples of their degree of dependency and interaction (Fig. 2.2). These include: (a) the Levins metapopulation, where population sizes are nearly

equal and all populations interact and habitats are patchy within the range

area; (b) the core-satellite (Boorman and Levitt, 1973) metapopulation

where habitats are patchy within the range, but one major population is

the source of fringe populations; (c) the patchy population, where habitats

are continuous throughout the species range, but local populations are aggregated; (d) non-equilibrium population, which is like the Levins model

except that there is no movement between local populations; and (e) an intermediate model between (b) and (c). According to Harrison (1991) the

dominant metapopulation structure is that of a large local population in a

large favorable habitat patch, surrounded by relatively unstable populations

in smaller habitat patches. This is similar to the mainland/island population

structure of MacArthur and Wilson’s (1967) theory of island biogeography.

In the metapopulation view, local subpopulations are connected by dispersal, which include larval dispersal and colonizing movements of adults.

Migrations, which are movements of individuals coordinated in space and

time (Quinn and Brodeur, 1991), can be ontogenetic, seasonal, or daily.

These migrations are distinguished from dispersal or nomadic behavior,

which is undirected and out of the natal or home range. Dispersal can

occur due to environmental factors, such as El Ni ̃no events, and also due to

density-dependent effects. As demonstrated for some fishes, fidelity to home

range depends on habitat quality (Matthews, 1990), which can depend on

density. The advantages of dispersal are colonization of new habitats and

avoidance of unfavorable local conditions (Quinn, 1993). The effectiveness
Bering Sea FOCI Final Report 9

Figure 2.2: Different kinds of metapopulations. Closed circles represent habitat patches; filled = occupied,

unfilled = vacant. Dashed lines indicate the boundaries of populations. Arrows indicate dispersion or migration (colonization). (a) Levins metapopulation. (b) Core-satellite metapopulation. (c) Patchy population.

(d) Non-equilibrium metapopulation. (e) An intermediate case that combines (b) and (c) (from Harrison,

1991).
10 S.A. Macklin (ed.)

of movement between populations depends on the extent of the movement

and the mortality of the dispersing individuals.

One of the major issues of the subpopulation concept is the fidelity to a

home range or natal site (natal philopatry). Through natal homing, animals

that stray away from their natal site may return for reproduction. In many

fishes where juveniles and adults make seasonal and ontogenetic migrations

related to feeding or reproduction, they may utilize either of three mechanisms, or a combination thereof, to return to their natal site and maintain

philopatry including: (1) imprinting on environmental cues, (2) learning

from other fishes (social tradition), or (3) genetically based homing. The

nature of the homing mechanism, when it occurs, has some interesting implications for management issues, as discussed below.

2.2.3 Genetic Structure

How populations are organized as metapopulations and their genetic structure are closely linked; genetic structure being determined by the amount

of gene flow between local populations. There are widely differing opinions

on the degree of structure in marine fish populations, ranging from a lot

of subpopulation structure to almost none. At one end is Sinclair’s (1988)

member/vagrant hypothesis, whereby there are many discrete populations,

genetically distinct through larval retention and mortality of vagrants. This

concept was founded on observations of specific spawning locations that seem

to favor retention of larvae. At the other end of the spectrum is Smith et

al. (1990) whose dynamic population concept has stocks with no discrete

genetic status as homogeneous isolates, but as dynamic heterogeneous components of the species; some genetic differences may occur from isolation by

geographical distance and gene selection. This concept arises from observations of high genetic variability within an area and low genetic differentiation

between areas.

Genetic divergence among subpopulations is promoted by mutation, genetic drift, and natural selection favoring adaptation to local environments

and hindered by the homogenizing process of gene flow from movements of

gametes, individuals, or populations (Slatkin, 1987). Phenotypic and genotypic characteristics have been used to distinguish fish subpopulations. The

use of phenotypic characters is still widely practiced, but when used alone is

generally received with some skepticism because phenotypes are influenced

by environmental conditions as well as genetic makeup. Biochemical and

molecular genetic techniques are powerful tools for fisheries; there have been

many studies of protein polymorphisms and more recently molecular genetics, looking for differences between nearby geographical populations, with

the goal of finding genetically isolated management units. Many studies of

marine fishes fail to distinguish populations (Pawson and Jennings, 1996),

either due to the state of technology as applied to population genetics, high

levels of gene flow, either historical or ongoing, or poor resolution power due

to small sample sizes (Taylor, 1991b). However, there have also been some

great successes, e.g., distinguishing smelt populations on opposite sides of

the St. Lawrence River (Bernatchez and Martin, 1996), mosquito fish pop-
Bering Sea FOCI Final Report 11

ulations within several hundred meters of shoreline (Kennedy et al., 1986),

and Fundulus populations along coastal transects (Gonzalez-Villasenor and

Powers, 1990).

In marine fishes, the importance of larval dispersal on gene flow and

population structure has been shown by several studies (Waples, 1987; also

see Avise, 1994). For example, Doherty et al. (1995) used isozymes to show

that a reef species Acanthochromis polycanthus, whose offspring are reared

in the parental territory and lacks larval dispersal, demonstrates negligible

gene flow over ca. 1000 km. Doherty showed that other species with larval

dispersal had genetically homogeneous subpopulations resulting from gene

flow. However, high dispersal potential may not always translate into high

gene flow and genetic homogeneity. There may be physical impediments to

dispersal, such as retention mechanisms, early life stages may not be passive

drifters, and later stages may have natal homing mechanisms.

There are several points of controversy about genetic differentiation, the

most critical and pervasive being the selective neutrality of genes, about

which there is still a lot of controversy (Gauldie, 1991; Avise, 1994; Rand,

1996). Hedgecock (1994) has noted a high degree of heterogeneity on a microgeographic scale for some marine fish and invertebrate species and has

proposed that a linkage between oceanographic conditions and variance in

reproductive success of marine animals is related to genetic heterogeneity.

Thus microgeographic heterogeneity results from temporal variation in the

genetic composition of recruits due to selection on larval populations matching survival windows of favorable oceanographic conditions, or to geographic

heterogeneity in the environment.

The level of genetic diversity in the population is also important for

successful population differentiation. For some species, both allozymes or

mtDNA may have a low degree of allelic variation (Bentzen et al., 1997).

For example, in western Atlantic cod Carr et al. (1995) found that 80% of

samples for cyt-b gene in mtDNA were of one haplotype, with the remaining

20% split between 16 other haplotypes. Differences between populations are

determined by the statistical differentiation of the frequency distribution of

a few rare haplotypes. Low levels of diversity in marine fish populations have

been attributed to historical bottlenecks or recent founding of the population

relative to the rate of mutation and genetic drift detectable in the particular

genetic structure (mtDNA, microsatellite, etc.) analyzed.

New techniques look promising for distinguishing subpopulations.

Bentzen et al. (1997) have applied nuclear DNA microsatellite analysis to

examine stock structure of western Atlantic cod. Previous studies using allozymes and mtDNA had limited success in differentiating cod stocks, but

Bentzen et al. (1997) found multiple stocks using their technique. Microsatellite DNA sequences appear to have high resolution for stock structure analysis due to the high rate of change in these regions of the DNA molecules, the

degree of allelic variation, and the likelihood that selection may be a minor

factor in determining microsatellite allele frequencies (Wright and Bentzen,

1994). Selection may promote or discourage population differentiation, and

since microsatellites are noncoding regions of the genome, polymorphisms

may be bound by structural contraints since there isn’t a protein product.
12 S.A. Macklin (ed.)

2.3 Characterization of Pollock

2.3.1 Distribution and Population Ecology

The walleye pollock is a species with a very broad niche. Although commonly associated with the outer shelf and slope regions of oceanic waters,

as a species it is capable of utilizing a wide variety of habitats including

nearshore eelgrass beds (J. Norris, School of Fisheries, University of Washington, Seattle, WA 98195, personal communication), large estuaries like

Puget Sound, coastal embayments, and open ocean basins such as the Aleutian Basin of the Bering Sea. Although adults of the species are often described as semidemersal, in some areas they are strictly pelagic (Bakkala,

1993). Pollock commonly feed on a wide assortment of prey from pelagic

copepods to epibenthic organisms, and pelagic and demersal fishes.

Pollock has an extremely broad range from Puget Sound to the northern

Bering Sea and on across the North Pacific Ocean (Fig. 2.3); it is most

abundant in the eastern Bering Sea and the Sea of Okhotsk. In addition

to an extensive range, the local abundance of pollock is usually high, often

dominating regional groundfish communities. Given its ecological plasticity,

broad range, and high levels of abundance, pollock appear to be a classical

generalist species capable of invading and adapting to marginal habitats.

The distribution of pollock is closely linked to temperature. The vertical distribution of juvenile pollock, and schools of adults and juveniles are

influenced by fronts, temperature, and depth (Bailey, 1989; Swartzman et

al. 1994). Interaction of temperature with behavior of pollock has been

well-studied (Olla et al. 1996; Sograd and Olla, 1996). The horizontal distribution of pollock is limited by cold temperatures, from 0◦ to 2◦, as shown

by distribution of commercial catches, and catches of juveniles and adults

in research surveys (Francis and Bailey, 1983). Detailed studies have not

been conducted at high temperatures, but the range of pollock appears to

be limited by temperatures of 10◦ to 12◦C.

We tracked the distribution pattern of several year classes in the eastern

Bering Sea to examine ontogenetic dynamics in distribution of different year

classes. The 1982 year class was found predominantly in the outer shelf

region of the southeast Bering Sea as larvae (Fig. 2.4a); as age-0 juveniles

they had moved northward and inshore (Fig. 2.4b). As age-1 fish, they

had distributed themselves farther northward, and also a large portion of

the population was found shoreward (Fig. 2.4c). As age-3 fish in summer, a

portion of the 1982 year class returned to the southern outer shelf region, but

a large number of fish remained in the northeast outer shelf (Fig. 2.4d). The

1989 year class was not sampled as larvae, but as age-0 juveniles in summer

it was broadly distributed across the middle shelf in the south and along the

outer shelf region in the northwest (Fig. 2.5a). This pattern persisted for age1, age-2, and age-3 fish (Figs. 2.5b–d). Portions of the year class distributed

inshore tended to persist there through age-3. The 1993 year class was

sampled as larvae along the outer shelf region of the south (Fig. 2.6a). It

was not sampled as age-0 juveniles, but as age-1’s was found far northward

in a band extending along the northern outer shelf (Fig. 2.6b, c). The
Bering Sea FOCI Final Report 13 Figure 2.3: The distribution range of walleye pollock shown with cross-hatching. Major spawning locations are shown with closed circles.
14 S.A. Macklin (ed.)

Figure 2.4: Relative distribution patterns of the 1982 year class of walleye pollock in the eastern Bering

Sea: (a) larvae in June from ichthyoplankton surveys, (b) age-0 juveniles in autumn from midwater trawl

surveys, (c) age-1 in summer from bottom trawl surveys, (d) age-3 in summer from bottom trawl surveys.

Contour shows area of highest abundance. Dashed line shows approximate region surveyed.
Bering Sea FOCI Final Report 15

Figure 2.5: Relative distribution patterns of the 1989 year class of walleye pollock in the eastern Bering

Sea: (a) age-0 juveniles in summer from midwater trawl surveys, (b) age-1 in summer from bottom trawl

surveys, (c) age-2 in summer from bottom trawl surveys, (d) age-2 in summer from midwater trawl surveys,

(e) age-3 in summer from bottom trawl surveys. Contour shows area of highest abundance. Dashed line

shows approximate region surveyed.

distribution of age-3 fish appears similar to that of age-2, perhaps with a

slight shift southward (Fig. 2.6d). Overall, these patterns indicate generally

northward movements of age-0 and age-1 fish. However, there appears to be

considerable interannual variability in distribution patterns; sometimes these

age groups move shoreward also. By age-3 it appears that pre-spawning fish

shift their distribution southward again.

Characterization of pollock as a colonizing species lends some support to

historical suggestions that the rapid increase in pollock populations occurring in the late 1960s was due to an “ecological release” caused by harvesting

off the competitive pressure of Pacific Ocean perch (Somerton, 1978) and decreases in abundance of Pacific herring. Under this scenario, pollock are a

classic r-selected species with opportunistic rapid growth, early maturity,

and high fecundity that were capable of rapidly taking over a niche opening; most likely, juvenile pollock were the stage capable of exploiting prey

resources made available. The expanding population of juveniles could have

made them the most available prey for pollock adults resulting in cannibal-
16 S.A. Macklin (ed.)

Figure 2.6: Relative distribution patterns of the 1993 year class of walleye pollock in the eastern Bering Sea:

(a) larvae in May from ichthyoplankton surveys, (b) age-1 in summer from bottom trawl surveys, (c) age-1 in

summer from midwater trawl surveys, (d) age-3 in summer from bottom trawl surveys (age estimated from

length class). Contour shows area of highest abundance. Dashed line shows approximate region surveyed.
Bering Sea FOCI Final Report 17

ism in the eastern Bering Sea. In the Gulf of Alaska, an increase of pollock in

the mid-1980s coincided roughly with a regime shift occurring in 1977–1978

by Tsuji’s (1989) assertion that during times of increasing commercial catch

levels (and therefore abundance) pollock expand into adjacent waters. Likewise, Stepanenko (1997) reports range expansions of pollock in the Bering

Sea related to increasing abundance and warming temperatures.

Comparing the mean and variance of subpopulation abundances over

time can characterize how populations are controlled in different areas of

the species range. In the case of pollock, a plot of mean subpopulation

abundance versus variability shows a slope less than unity, indicating that

peripheral, less abundant pollock stocks vary more than central, more abundant stocks (Fig. 2.7). These results could either indicate more density dependence in the central stocks, including density-dependent colonization of

peripheral populations, or that environmental conditions are more variable

and have a greater effect on peripheral populations.

2.3.2 Year Class Dynamics

For all of the major pollock groupings stock fluctuations are strongly influenced by intermittent recruitment of strong year classes. For example,

Fig. 2.8shows the impact of a series of strong year classes on stock abundance in the Gulf of Alaska, as well as the drop in abundance related to

subsequent recruitment of relatively poor year classes. In the eastern Bering

Sea the 1978year class comprised 67% of the pollock population in 1981

and 53% of the population in 1982. Many regions share the same strong

year classes; for example, 1978was a strong year class in the Gulf of Alaska,

Aleutian Basin, eastern Bering Sea, western Bering Sea, and Sea of Okhotsk.

Likewise 1982, 1984, and 1989 were strong across the Bering Sea, although

not in the Gulf of Alaska. Strong year classes in the Gulf of Alaska including

1976, 1977, 1979, and 1988 did not appear strong in the Bering Sea. Therefore, although some strong year classes are shared, there is not a consistent

association of strong year classes among the Bering Sea and Gulf of Alaska

populations that would clearly indicate density dependent dispersal between

these geographic regions. However, within the Bering Sea there appears to

be an association of strong year classes among the different regions. The occurrence of similar strong year classes in different regions of the Bering Sea

has been cited as evidence of panmixia within the Bering Basin (Dawson,

1994). At the extreme ends of the range of pollock, e.g., Puget Sound, the

strong year classes (1972–1975) were quite different from those in the major

centers of abundance.

2.4 Population Structuring Mechanisms in Pollock

In fish populations, gene flow can occur as a result of movements of adult,

juvenile, or larval stages. Species with a high degree of adult vagility living in

fine-grained habitats often have little genetic structure in their populations

(Avise, 1994). As well, species like salmon, whose larvae have little opportunity to mix, attain whatever gene flow between major drainages by straying
18 S.A. Macklin (ed.) Figure 2.7: The standard deviation of pollock abundance against average abundance for seven stocks of walleye pollock, 1979–1991, showing that peripheral, less abundant stocks vary more than central, more abundant stocks. Upper line has a slope of unity, bottom line is regression line of stock data (slope = 0.864).
Bering Sea FOCI Final Report 19 Figure 2.8: Year class abundance as age-2 recruits (bars) compared to spawning biomass of walleye pollock in the western Gulf of Alaska (line), showing the dramatic effects of year class strength on population biomass.
20 S.A. Macklin (ed.)

and mixing of adult gene pools. In species whose adults and juveniles migrate widely, genetic structure may be maintained by natal homing, as is

well recognized in Pacific salmon. For other species as well, such as rainbow

smelt, natal homing ability seems quite remarkable (Bernatchez and Martin,

1996).

Walleye pollock provide an excellent opportunity to study different population structuring mechanims. Pollock appear to have immigrated to the

North Pacific within a period between the submergence of the Bering Sea

land bridge and the coming of the ice age, about 3–5 million years ago (Svetovidov, 1948). In fact, the earliest records of gadids in the North Pacific are

found in Pliocene sediments off the California coast. Pollock spawning populations are now found across the rim of the North Pacific Ocean from central

Japan to Puget Sound. Larger populations are contained in the major basins

of the Bering Sea and Sea of Okhotsk, but smaller populations are found in

many bays, fjords, and sea valleys along the continental shelf. During the

last period of major glaciation about 10,000–18,000 years ago, when sea levels could have been as much as 150 m lower than present day levels, the

major basins were substantially more isolated with strong geographical barriers between populations. Many of the fjords presently inhabited by pollock

would have been in the process of being scoured by glaciers. Consequently,

pollock stock differentiation could have occurred by several mechanisms, including founder effects and genetic drift of small re-colonizing populations

in the fjords, loss of genetic diversity by population bottlenecks, isolation by

barriers and by distance combined with selection, and genetic drift.

Pollock have been the subject of studies of larval transport in relation to

oceanographic conditions in the Gulf of Alaska since 1981 (Kim and Kendall,

1989). Pollock eggs and larvae are found in large aggregations that can be

tracked and monitored (Bailey et al., 1996b) and their distribution can be

predicted reasonably well from ocean currents. Pollock larvae are also associated with oceanographic features such as eddies (Vastano et al., 1992;

Schumacher et al., 1993). Larval abundance levels are correlated with environmental conditions related to transport (Bailey and Macklin, 1994) and

recruitment levels of the population have been linked to events during early

life history (Bailey et al., 1996a). In the following section, I discuss the role

of variability in larval transport and retention by features, such as eddies,

in mortality and genetic structuring of the walleye pollock population, and

explore the possible linkages between them. These linkages are made using

both published and original sources of data. Other mechanisms of population

structuring in pollock are discussed, with the main emphasis on populations

in the Bering Sea and Gulf of Alaska.

2.4.1 Regional Oceanography and Transport

In the Gulf of Alaska, the major spawning of pollock is in Shelikof Strait,

a deep sea valley (>250 m) penetrating the continental shelf between the

Alaska Peninsula and Kodiak Island. Flow in this region is dominated by the

Alaska Coastal Current, which is one of the most vigorous coastal currents

in the world with speeds of 25–100 cm s−1 (Stabeno et al., 1995). The
Bering Sea FOCI Final Report 21

Alaska Coastal Current bifurcates east of Sutwik Island, with one branch

continuing along the shallow continental shelf (∼100 m) along the Alaska

Peninsula. This branch has relatively weak flow, with speeds of about 10

cm s−1. The other branch flows seaward through the sea valley with a

portion that joins the Alaska Stream (with speeds of 50–100 cm s−1) and

the remainder recirculating onto the shallow shelf.

Frontal features, meanders, and eddies are prominent in the Shelikof sea

valley (Vastano et al., 1992; Napp et al., 1996). Horizontal density gradients

and vertical shear in the flow result in baroclinic instabilities, which generate

eddies in the region. The location of eddy formation coincides with the area

of pollock spawning (Schumacher and Kendall, 1995), and in the springtime

spawning period three to four eddies form per month (Bograd et al., 1994),

some of which may remain stationary for weeks (Schumacher et al., 1993).

In the Bering Sea a cyclonic gyre dominates circulation, with the Kamchatka Current flowing southward along the western side and the Bering

Slope Current northward along the eastern side of the central Aleutian Basin.

Alaska Stream water can enter the Aleutian Basin through any of the deep

Aleutian passes, but predominately through Amchitka, Amutka, and Buldiur

Passes, and Near Strait. The transport through the passes varies on time

scales of months. Over the main area of our interest, the southeast basin

and the shelves, the flows of interest are the Bering Slope Current (BSC)

and Aleutian North Slope Flow (ANSF). The ANSF flows eastward along

the north slope of the Aleutian Islands and connects flow through the passes

with the BSC. Instabilities in the BSC can result in onshelf flow from the

basin onto the shelf.

The shelf is divided into three regions, the inner shelf (depth <50 m),

the middle shelf (50–90 m), and the outer shelf (100–170 m). Flow on the

middle shelf is very weak (mean flow <1 cm s−1). Stronger flows occur at

the transition zones between the inner middle shelf and the middle outer

shelf. Flow along the 100-m isobath is generally northwestward at ∼5–

10 cm s−1, while the northeastward flow along the 50-m isobath is weaker

at ∼2–3 cm s−1 (Schumacher and Stabeno, 1997). Flow along the 100-m

isobath originates from onshelf flow from the basin and from flow through

Unimak Pass. The flow along the 50-m isobath originates from the flow

through Unimak Pass.

Eddies in the eastern Bering Sea are relatively common (Schumacher

and Stabeno, 1994), and are formed in regions of high current shear, or by

the interaction of inflowing Alaskan Stream water with topography. Eddies

that may transgress the continental shelf break up in shallow water over a

period of days. Eddies may circulate vigorously (25 cm s−1), but their net

movement is generally slow (1–5 cm s−1). Diameters of eddies may vary

from 5–80 km.

2.4.2 Larval Transport, Eddy Retention, and Mortality

Pollock spawn at predictable times and locations, generally in sea valleys,

canyons, or indentations in the outer margin of the continental shelf; but

they are also known to spawn in very deep water over the Aleutian Basin
22 S.A. Macklin (ed.)

and in fjords (Fig. 2.3). These locations are known to be repeat spawning

areas, year after year. In Shelikof Strait, Alaska spawning occurs during the

last week of March and the first week of April. In the Bogoslof Island region

in the Aleutian Basin, pollock spawn in late February to early March, and

over the southeastern Bering Sea shelf most fish spawn from mid-April to

May. Depending on the region, eggs are spawned deep in the water column

(100–400 m) and after hatching the larvae are located in the upper portion

of the water column (generally from 20–60 m depth).

In Shelikof Strait, pollock show a mean downstream progression of their

center of abundance over time (Fig. 2.9). However, there is a great deal of interannual variability within these mean patterns. Larval transport patterns

show good correspondence with satellite-tracked drifter patterns. In years

when larvae are transported onto the shallow shelf west of the sea valley,

larvae drift downstream at speeds of 4 to 6 cm s−1 (Hinckley et al., 1991).

About 70 satellite-tracked drifters drogued at 40 m to simulate larval

drift have been released in the Shelikof sea valley. The drifters show the

pattern of bifurcation of the ACC and the variability in fate of larvae during

the 50 d or so when they are planktonic (Fig. 2.10). Residence time of the

drifters on the shelf ranges from 35–122 d, with a mean of 55 d. Drifters can

exit the sea valley in about 15 d and enter the Alaska Stream where they

are quickly transported westward.

Eddies in the Shelikof Sea Valley can retain larvae for several weeks in the

region. In 1990 an eddy was found with an aggregation of larvae (Fig. 2.11).

Satellite-tracked drifters remained in the eddy for ∼22 d, until the eddy

moved westward, and interacted with shallow topography of the shelf and

disintegrated.

The role of eddies in larval mortality is not completely understood. Eddies early in the spawning season before peak larval abundance have been associated with enhanced phytoplankton and zooplankton concentrations, and

enhanced larval feeding and nutritional condition (Canino et al., 1991; Napp

et al., 1996). However, the eddy in 1990 had similar microzooplankton concentrations, larval feeding, and condition compared to regions sampled outside the eddy, and mortality rates in the eddy were not significantly different

from mortality rates calculated for the whole sea valley region (0.05–0.07 d−1

in eddy based on birthdate cohorts: Bailey, unpublished data; 0.04–0.11 d−1

for whole region: Bailey et al., 1995). How larvae are entrained in eddies is

not well understood. Birthdate distributions of larvae within the 1990 eddy

sampled about 20 d apart indicate that larvae continue to be recruited into

the eddy well after it is formed, which complicates mortality calculations

based on the conservation of properties within the eddy (Fig. 2.12).

In some years with strong and frequent storm activity, wind-driven transport increases and flushes most larvae from the sea valley into the Alaskan

Stream. An excellent example of this is 1991; winds were extremely high,

with three storm events during the late April early May period, and drifter

trajectories indicated that most water vigorously flowed out the sea valley

(Fig. 2.13). Under these conditions, primary production and microzooplankton levels were depressed, larval feeding and nutritional conditions were poor,
Bering Sea FOCI Final Report 23 Figure 2.9: Centroids of larval pollock distribution tracked by month, averaged over 1987–1992.
24 S.A. Macklin (ed.) Figure 2.10: Composite of representative satellite-tracked drifter trajectories in the Gulf of Alaska. Drifters were drogued at 40 m, released near larval pollock aggregations and pathways tracked for 50 d, approximating the duration of larval drift.
Bering Sea FOCI Final Report 25

Figure 2.11: Distribution of walleye pollock larvae during late May 1990. Lines are satellite-tracked drifter

trajectories from releases on the larval patch in early May. Units in catch 10 m−2.
26 S.A. Macklin (ed.)

Figure 2.12: Hatchdate distributions determined from otolith increment counts and day of capture for (a)

larvae sampled at stations within the eddy in early May 1990, and (b) larvae sampled at stations within the

eddy in late May 1990.
Bering Sea FOCI Final Report 27

Figure 2.13: Distribution of walleye pollock larvae during late May 1991. Lines are satellite-tracked drifter

trajectories from releases on the larval patch in early May. Units in catch 10 m−2.
28 S.A. Macklin (ed.)

and larval mortality was high (Bailey et al., 1995). In general, larvae experiencing conditions associated with high transport will have low survival.

There are limited data to compare larval condition in the Alaskan Stream

water compared to other areas. However, microzooplankton levels are relatively low compared to nearshore stations (Bailey et al., 1995) and larval

growth rates are significantly lower than for larvae found over the shelf region. In 1991, the few surviving larvae that were caught at offshore stations

had significantly lower growth rates than larvae caught in the sea valley (0.14

mm d−1 compared to 0.20 mm d−1; P < 0.05).

In the eastern Bering Sea, larval pollock concentrations have not been

tracked as effectively as in the Shelikof region. There are several areas where

repeated spawning is known to occur (Fig. 2.14) and where larvae are frequently concentrated. From drifter studies it appears that larvae from different areas can readily mix during the larval drift period. About 80 satellite

tracked drifters have been released in the Bering Sea to study potential larval

drift patterns (typical patterns are shown in Fig. 2.15). On the middle shelf

area (50–100 m depth) the flow is weak and all drifters remained resident

there for more than 60 d. Drifters released in the Unimak Pass spawning

region are either transported along the 100-m isobath until reaching the Pribilof Islands, at which time they may circle the islands, flow eastward across

the shelf along the 50-m isobath, or continue northward to St. Matthew Island. Residence time in the slope region is 30–90 d, with a mean northward

velocity of 5 cm s−1. Drifters released near Bogoslof Island usually follow

the ANSF into the BSC. Although about 15% of drifters go onto the shelf,

drifters in this area may re-circulate in a small sub-gyre in the southeast

corner of the Aleutian Basin.

There are eddies in the Bering Sea similar to those in Shelikof Strait

that may act as larval retention mechanisms (Fig. 2.16). An eddy found

in 1993 over the southeastern corner of the Aleutian Basin was associated

with very high numbers of larvae; however, it later entered the outer shelf

and disintegrated, providing a vehicle for mixing of larvae between spawning

regions.

The Aleutian Basin region may act as a geographical barrier to gene flow

across the Bering Sea. Microzooplankton concentrations are low and larval

feeding levels are also low compared with other regions (Hillgruber et al.,

1995; Theilacker et al., 1996). Furthermore, studies of larval mortality done

in the basin region indicate relatively low larval growth rates and potential

for high levels of mortality (Dell’Arciprete, 1992).

2.4.3 Migration Patterns and Philopatry

Other mechanisms of maintaining population structure include philopatry

and natal homing. Pollock show repeated and predictable spawning at specific sites and times, which is one piece of evidence for natal philopatry.

Some of these persistent spawning sites are shown in Fig. 2.3. Among the

best studied spawning aggregations is that in Shelikof Strait which has been

monitored since 1981; the Shelikof Strait spawning aggregation is the largest

spawning biomass in the Gulf of Alaska, and mostly spawns within a lim-
Bering Sea FOCI Final Report 29

Figure 2.14: Major areas of spawning and larval concentrations in the eastern Bering Sea (shaded area).
30 S.A. Macklin (ed.) Figure 2.15: Composite of representative satellite-tracked drifter trajectories in the Bering Sea. Drifters were drogued at 40 m, released near larval pollock aggregations or on spawning grounds and pathways tracked for 50 d, approximating the duration of larval drift.
Bering Sea FOCI Final Report 31 Figure 2.16: Distribution of walleye pollock larvae in April 1993 in the eastern Bering Sea. Also shown are satellite- tracked drifter trajectories showing location of eddy in the region.
32 S.A. Macklin (ed.)

Figure 2.17: Recapture distribution for experiment in which 666 pollock were tagged and released (triangle)

in the northern Sea of Japan on April 17, 1968. Locations and dates of recaptures are shown by closed cirlces.

H: Hokkaido Island, S: Sakhalin Island (from Tsuji, 1989).

ited area (40 km × 80 km) during the first week in April (Kendall et al.,

1996). The geographic and temporal consistency of spawning for this and

other spawning aggregations argues against the notion that the timing and

position of spawning is random, depending on suitable conditions.

Mark-recapture studies around Japan where pollock were tagged during

the spawning season (April) showed dispersed feeding migrations but return

homing to specific previous spawning locations (Tsuji, 1989; Fig. 2.17). In

other studies, pollock tagged during the summer feeding periods were later

recaptured across a wide geographical expanse (Fig. 2.18). Those recaptured

around the time of the spawning season were located near well-established

spawning grounds. Pollock appear to widely disperse after spawning, and

the location of summer feeding grounds may vary. The fact that fish tagged

in summer in the western Bering Sea were recaptured in the eastern Bering

Sea, along with the significant population differentiation between eastern

and western Bering Sea spawning pollock discussed below, indicates isolation

of spawning groups even though they may mix during the summer feeding

period. While not unequivocally proving natal spawning, the persistence of

spawning locations over time (Fig. 2.3) and repeat spawning are two elements

of natal philopatry.
Bering Sea FOCI Final Report 33 Figure 2.18: Movement of walleye pollock tagged by Japanese scientists in the Bering Sea (from Dawson, 1994). Note: most tagging and recoveries occurred during the summer/autumn feeding season. Note cluster of April recoveries near Unimak Pass in the spawning season.
34 S.A. Macklin (ed.)

Table 2.2: Summary studies of pollock stock structure using phenotypic characteristics.

Author Method Area Results

Ogata (1959) meristic—vertebrae

counts

Sea of Japan and Pacific

Ocean side of Japan

Sea of Japan has 3 different

stocks. Sea of Japan differs

from the Pacific Ocean side.

Iwata and Hamai

(1972)

meristic—vertebrae

counts

Sea of Japan, Okhotsk Sea,

and Pacific Ocean near

Hokkaido

8 “local forms”—

2 groups in the Sea of Japan

3 groups in the Okhotsk Sea

3 groups in the Pacific Ocean

Hashimoto and Koyachi (1969)morphometrics—body

length and other

morphological features

northern Japan 3 groups discriminated

Janusz (1994) meristics and morphometricSea of Okhotsk 3 stocks distinguished

Temnykh (1991) morphometrics Sea of Okhotsk S. Kurils population distinguished from N. Sea of Okhotsk

Temnykh (1994) morphometrics W. Bering Sea and E.

Kamchatka

W. Bering and E. Kamchatka

stocks distinguished

Ishida (1954) morphometrics—

otoliths

northern Sea of Japan,

Okhotsk Sea, and northern Pacific Ocean coast of

Japan

Otolith size is larger in Sea

of Japan pollock than Okhotsk

Sea. Otoliths are similar between Sea of Japan and Pacific

Ocean pollock.

Shaw and McFarlane

(1986)

morphometrics—

length-at-age

British Columbia—Dixon

Entrance, Strait of Georgia

2 stocks discriminated—Strait

of Georgia pollock are smaller.

Little interaction between pollock north and south of Queen

Charlotte Sound.

Thompson (1981) morphometrics—

length-at-age

British Columbia—Dixon

Entrance, Strait of Georgia, Queen Charlotte

Sound

3 separate stocks—each area

contains its own distinct stock.

Little mixing occurred between

them.

Saunders et al. (1989) morphometrics, life historyBritish Columbia Separate stocks in Strait of

Georgia, Hecate Strait/Dixon

Entrance, Queen Charlotte

Sound and W. Vancouver I.

Lynde et al. (1986) morphometrics—

length-at-age

eastern Bering Sea and

Bering Sea basin

northeastern shelf and slope

and Aleutian Basin represent

one stock distinct from other regions of the eastern Bering Sea

Hinckley (1987) spawning time and location; morphometrics

—length-at-age; fecundity

Aleutian Basin and eastern

Bering Sea shelf and slope

3 spawning stocks in the eastern Bering Sea—basin, northeastern slope and eastern shelf

and slope
Bering Sea FOCI Final Report 35

Table 2.2: (continued).

Author Method Area Results

Mulligan et al. (1989) spawning time and locationeastern Bering Sea and

Aleutian Basin

three spawning areas separated

in space and time: EBS SE

Shelf, EBS NW shelf, Aleutian

Basin

Serobaba (1977) morphometrics and

meristics

northern, western, eastern

and southern Bering Sea

different stocks occupy each region

Dawson (1994) morphometrics Bering Sea Three stocks—eastern Bering

Sea shelf, Aleutian Basin, and

Aleutian Islands

Janusz et al. (1989) meristics and morphometricsDonut hole and eastern

Bering sea shelf

2 stocks distinguished in Donut

Hole and eastern Bering Sea

Nitta and Sasaki (1990) morphometrics Donut hole, eastern Bering

Sea, near Japan

Characteristics distinguish 3

stocks, with about 90% classification accuracy

Gong et al. (1990) meristics Asian and Bering Sea Asian and Bering Sea stocks

distinguished but stocks within

these regions not distinguished

Wilimovsky et al.

(1967)

meristic (fin ray and

vertebral counts) and

morphometric

entire Pacific Ocean morphometric—no strong evidence for discrete stocks.

meristic—no differences between Bering Sea and Puget

Sound pollock. No differences

between Gulf of Alaska and

Northern B.C. pollock.

Koyachi and Hasimoto

(1977)

meristic—fin ray, gill

raker, and vertebrae

counts

entire Pacific Ocean 12 subpopulations, including

the Bering Sea and Gulf of

Alaska

2.4.4 Genetic and Metapopulation Structure

We have summarized studies on stock structure of pollock according to their

phenotypic, acquired, or genetically based nature. Briefly, phenotypic characteristics of pollock, such as meristic or morphometric measurements, both

within small geographic regions and across much broader areas, have indicated considerable population structure (Table 2.2). For example, Koyachi and Hashimoto (1977) used differences in vertebral, gill raker, and fin

ray counts to distinguish 12 groups of pollock across its range. Within

much smaller geographic regions there are also distinct groups. For example, around the islands of Japan and Sea of Okhotsk, Iwata and Hamai

(1972) identified eight groups, and in the Sea of Okhotsk three stocks were

distinguished (Janusz, 1994). Within the eastern Bering Sea, including the

eastern Aleutian basin, three to five stocks have been distinguished using

morphometrics and life history characters (Lynde et al., 1986; Hinckley,
36 S.A. Macklin (ed.)

1987; Dawson, 1994). Gulf of Alaska and Bering Sea populations appear to

be phenotypically differentiated (Koyachi and Hashimoto, 1977). For example, Koyachi and Hashimoto (1977) and Hashimoto and Koyachi (1977) used

differences in vertebral counts and in growth rates to distinguish 11 groups

of pollock across its range. Within a small area, for example around the

islands of Japan, there are also distinct groups (Iwata and Hamai, 1972).

Naturally acquired tags, such as elemental composition of otoliths and

parasite characteristics, indicate restricted mixing among pollock juveniles

and adults of different subpopulations (Table 2.3). For example, the chemical

“fingerprint” of otoliths near the nucleus (deposited during early larval life)

could be utilized to assign fish to their capture location as juveniles with

70–85% accuracy over broad regions of the eastern Bering Sea (Mulligan

et al., 1989), indicating limited movement and mixing of fish from different geographic regions. Using parasite frequencies, adult pollock caught on

the south side of Vancouver Island can be distinguished from those on the

west side with about 75% accuracy (Arthur, 1983). In the Sea of Okhotsk,

several different populations of pollock were distinguished based on parasite frequencies (Avdeev and Avdeev, 1989). By contrast, mark-recapture

studies where pollock were tagged in summer indicate broad movement of

individuals across areas of the Bering Sea (Fig. 2.18). However, critical studies of marking spawning pollock have not been conducted. Tagging results

thus far indicate potential for dispersal during the summer feeding period.

Historical tagging studies do not provide information indicating whether individuals are moving with large schools as migrating populations, whether

individuals are vagrants and mixing with local populations, or if dispersal

patterns in the Bering Sea are part of ordered seasonal migrations. Tagging

studies around Japan do support dispersed feeding migrations and homing

migrations to specific spawning areas (Tsuji, 1989).

Studies using biochemical and molecular methods on pollock show mixed

results for distinguishing stock structure of pollock, varying somewhat by

technique (Table 2.4). Using allozymes, Grant and Utter (1980) detected

minor differences between the Gulf of Alaska and Bering Sea, but no differences within either region. Using mtDNA sequence data from a 276 bp

spacer sequence near the cytochrome b gene, and the left side of the control

region, Shields and Gust (1995) reported slight genetic differences between

eastern and western Bering Sea pollock. However, the season samples were

acquired was not reported; if samples were collected in the summer feeding

season when stocks may be mixed, genetical resolution can be blurred. The

relatively small size of the control region of pollock mtDNA, lack of length

mutations within the control regions sequenced to date, and the very low

transition to transversion ratios of the control and spacer regions (1.2:1.0 and

1.29:1.0, respectively) suggest that these regions may not be variable enough

to provide greater genetic discrimination among populations. Mulligan et al.

(1992) employed mtDNA RFLP on fish collected during the spawning season

and distinguished among stocks in the Gulf of Alaska, Donut Hole/Bogoslof

Island, and Aleutian Island. Profiles from nine restriction enzyme digests

yielded 65 composite genotypes. Pairwise comparisons of Gulf of Alaska ver-
Bering Sea FOCI Final Report 37

Table 2.3: Summary studies of pollock stock structure using acquired characteristics.

Author Method Area Results

Nakano et al. (1991) otolith chemistry:

adults, whole otolith

homogenates

eastern Bering Sea, western Bering Sea, Donut holedifferences in 3 areas, little mixing

Mulligan et al. (1989) otolith chemistry: juveniles, inner early life

otolith increments

eastern Bering Sea, (SE

Shelf, NW Shelf, Aleutian

Basin)

differences in 3 areas, some mixing

Severin et al. (1995) otolith chemistry: juveniles, outer otolith incrementseastern Bering Sea (Bristol

Bay), Gulf of Alaska

distinguish 5 areas, some mixing

Arthur (1983) parasites British Columbia—Strait

of Georgia, West side of

Vancouver Island, Queen

Charlotte Sound, and

Dixon Entrance

3 stocks in this area; Strait of

Georgia, Vancouver Island and

Queen Charlotte Sound/ Dixon

Entrance

Avdeev and Avdeev

(1989)

parasites Sea of Okhotsk, Kommader Is., Kamachatka

Penin.

Seven distinct groups within

the NE Sea of Okhotsk, distinct groups in Kommander I.,

E. Kamchatka, and Shirshov

Ridge

Misc. Authors, see

Figs. 2.17, 2.18.

Tagging studies western and eastern Bering

Sea, Japan

Broad movements, homing migrations to spawning site

sus the Bering Sea showed significant genetic differentiation between these

populations (Fig. 2.19).

More recently, using sequences of mtDNA cytochrome-b and ATPase-8,

Powers (1996) and his colleagues (J. Quattro and D. Powers, unpublished

data, Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950;

see Appendix 2a) identified haplotype differences between Asian and North

American pollock. The unique DNA sequences allowed them to develop

an enzyme method to rapidly identify individuals by RFLP. An analysis of

molecular variance on the combined data identified sharp distinctions between Asian and North American fish and considerable substructure within

the American and Asian clusters (Fig. 2.20).

A promising technique for examining genetic variance among fish populations is the study of genomic DNA microsatellites. Microsatellites are nuclear

DNA sequences comprising tandem arrays of di-, tri-, or tetranucleotide repeats such as (GT)n or (CAC)n that usually extend over less than 300 base

pairs (bp) (Wright and Bentzen, 1994). Microsatellites are dispersed at intervals of 10–30 kilobase (kb) intervals throughout eukaryotic genomes, and

alleles exhibit high levels of size variation associated with variation in the

number of repeating units. Hence, microsatellites constitute an extremely

abundant class of highly polymorphic genetic markers. Allelic variation in
38 S.A. Macklin (ed.)

Figure 2.19: UPGMA clustering of genetic distances among walleye pollock stocks in the eastern Bering

Sea and Shelikof Strait (from Mulligan et al., 1992).

microsatellites can be detected by using oligonucleotide primers specific to

DNA sequences flanking the satellite and amplifying between the primers

using the polymerase chain reaction. Alleles are discriminated by using

electrophoresis to separate the PCR products according to size in polyacrylamide gels. Studies of microsatellite markers in Atlantic cod populations

(Bentzen et al., 1996) have yielded finer genetic discrimination of geographic

subpopulations than had been possible previously. Powers and his colleague

Gary Villa (unpublished data, Hopkins Marine Station, Stanford University,

Pacific Grove, CA 93950; see Appendix 2a) screened populations for DNA

microsatellite loci that allowed the discrimination between pollock populations on a finer scale than was possible by mtDNA analysis. Using PCR

primers that allow amplification of microsatellites in Atlantic cod (Bentzen et

al., 1996), pairwise comparisons from the first two microsatellite loci examined, Gmo145 and Gmo2, confirmed differences between Asian and American

pollock stocks, and further resolved differences between Gulf of Alaska and

Bering Sea stocks (Fig. 2.21). However, in the case of Gmo145 there was a

null allele scored for this primer that was responsible for the major east-west

differences. The presence of a null allele indicates that nucleotide sequences

in the flanking regions of microsatellite markers are not homologous between

these populations, resulting in no scorable PCR product.

Microsatellite alleles may be “the most powerful Mendelian markers ever

found” (Jarne and Logoda, 1996). Microsatellites have a number of valuable
Bering Sea FOCI Final Report 39 Figure 2.20: UPGMA dendogram of walleye pollock stocks from mt-DNA RFLP data utilizing the DA-Genetic Distance Method of analysis (from Powers).
40 S.A. Macklin (ed.)Figure 2.21: UPGMA dendogram of walleye pollock stocks from microsatellite polymorphism frequencies from primers Gmo2 and Gmo145 (from Powers).
Bering Sea FOCI Final Report 41

Table 2.4: Summary studies of pollock stock structure using acquired characteristics.

Author Method Area Results

Mulligan et al. (1992) mtDNA RFLP eastern Bering Sea basin,

Aleutian Is.

and Gulf of Alaska

2 distinct stocks in Aleutian Is.

and Donut Hole/Bogoslof, Gulf

and Donut Hole/Bogoslof have

informative differences

Shields and Gust

(1995)

mtDNA sequencing across Bering Sea and Gulf

of Alaska

significant differences between

eastern and western Bering Sea

Grant and Utter (1980) allozyme southeastern Bering Sea

and Gulf of Alaska

minor genetic differences between the two areas. No differences within the areas.

Johnson (1977) allozyme eastern Bering Sea and

Gulf of Alaska

No significant differences found

Iwata (1973) allozyme northern Sea of Japan

and north Pacific coast of

Japan

No differences found

Iwata (1975a, b) allozyme northern Sea of Japan and

eastern Bering Sea

Highly significant differences

found between the two areas

Efremov et al. (1989) allozyme northern Sea of Okhotsk Allozyme variability suggesting

that aconitase could be genetic

marker

Powers (1996) mtDNA RFLP and

DNA microsatellite

Bering Sea and Gulf of

Alaska

eastern and western Bering Sea

distinguished using mtDNA,

Gulf of Alaska and eastern

Bering Sea stocks have informative differences using microsatellite DNA

attributes as tools in stock discrimination. First, they typically exhibit much

higher levels of variability than other conventional genetic markers, such as

allozymes or mitochondrial DNA. In marine fishes and invertebrates they

typically have 10 or more alleles, and heterozygosities of 50–95% (Wright

and Bentzen, 1994; Bentzen et al., 1996; Garc ́ıa de Le ́on et al., 1997). This

higher level of polymorphism may confer greater resolution in surveys of

population structure than that obtained with either allozymes or mtDNA, a

generalization supported both by theoretical analyses and several empirical

studies in which microsatellite surveys have revealed population structure

not evident with either allozymes or mtDNA (Bentzen et al., 1996; Ruzzante

et al., 1996a, b). As well, rates of change of microsatellites appear to be on

the order of 104 greater than those for coding DNA. These rates of change are

due to replication errors causing size polymorphisms rather than mutation

rates resulting in base pair changes. Second, microsatellites are more likely

to be selectively neutral than either allozymes or mtDNA, which increases
42 S.A. Macklin (ed.)

their value for estimating gene flow (migration) rates. Third, the DNA basis

of microsatellites, their small size and the use of PCR in their assay present

logistical advantages in sample acquisition (minimal tissue requirements and

no need for frozen storage) and makes possible the use of archival materials

such as scales and otoliths as tissue sources, hence making retrospective

studies a possibility.

An emerging view of genetic structure in walleye pollock suggests a more

complex pattern of stock structure than recognized previously. Studies to

date indicate varying degrees of genetic differentiation between pollock in

the Gulf of Alaska and Bering Sea. Phenotypic differences between stocks,

elemental composition of otoliths, and parasite studies are consistent with

this interpretation. Distinction between adjacent putative stocks at the subbasin scale, for example in the eastern Bering Sea, is currently lacking but

is more likely to be observed when higher-resolution molecular techniques

are used. Therefore, more pollock-specific microsatellite primers need to

be developed and tested to survey a greater number of microsatellite loci.

Although the microsatellite analyses presented here are tentative, they are

generally supportive of data from life history characteristics and phenotypic

patterns that indicate considerable population heterogeneity.

2.4.5 Discussion of Gene Flow and Larval Transport

Among the major basin regions of the Sea of Japan, Sea of Okhotsk, Bering

Sea, and Gulf of Alaska there is good evidence of genetic structure in pollock that is supported by genetic, phenotypic, and life history data. Probably

these major basin regions were largely isolated from each other during the

last major glaciation, as well as at other times during pollock’s ancient history in the North Pacific. Considering the colonizing ability of pollock the

potential limited degree of genetic mixing between populations is somewhat

surprising, but perhaps can be attributed to larval retention mechanisms,

differences in reproductive characteristics (timing and temperature adaptations), natal homing, or outbreeding depression of vagrants that reproduce

with historical local populations.

In spite of substantial opportunities for gene flow through larval transport

and dispersal of juveniles and adults within a major region like the Bering

Sea, there appears to be genetic differentiation of populations across a wide

distance, such as the eastern versus western Bering Sea. The inhospitable

nature of the Aleutian Basin as a nursery for larvae and juveniles may act

as a barrier to population mixing. Among adjacent spawning regions in

the eastern Bering Sea, the potential for gene flow during larval drift is

high. However, since there appears to be an unresolved degree of structuring

within the Bering Sea, reduced gene flow due to larval retention mechanisms

or strong natal homing and philopatry may be indicated.

Genetic differentiation between the Gulf of Alaska and Bering Stocks

presents an interesting scenario. The Alaska Peninsula presents an obvious

land barrier to mixing. Larvae spawned in Shelikof Strait are frequently retained in the sea valley region by fronts and eddies, and larvae transported

onto the shallow continental shelf between the Shumagin Islands and the
Bering Sea FOCI Final Report 43

Shelikof sea valley have a long residence time there due to slow and meandering currents. Years with conditions that favor transport into the Alaska

Stream are also years of high larval mortality. When larvae do enter the

Alaskan Stream, where they could be transported into the Bering Sea, they

encounter conditions that are poor for survival. Furthermore, the transit

time is usually greater than the 50 d planktonic life of larvae. If larvae did

survive the journey in the Alaskan Stream, they would enter the Bering Sea

through the relatively deep western island passes. To mix with the gene pool

on the eastern Bering Sea shelf, they would have to cross the Aleutian Basin

region, where feeding conditions are poor and mortality is high. Unimak

Pass is the only conduit between the shelf of the North Pacific and eastern

Bering Sea. While several drifters deployed in Shelikof Strait have entered

the Bering Sea through Unimak Pass, the transit time exceeded 60 d in each

case. Consequently, it appears that vagrants from the Shelikof Strait spawning have a high mortality, limiting gene flow and population homogenization

between the Gulf and Bering populations. These populations could have

become differentiated during isolation by glaciation and founder effects, or

alternatively, during recent periods of bottlenecks and genetic drift. Whereas

the Bering Sea pollock population is extremely large and unlikely to experience genetic drift, the Gulf of Alaska population is smaller and is known to

fluctuate widely, perhaps experiencing periods of enhanced genetic drift.

2.4.6 Metapopulation Summary

A summary view of genetic structure in walleye pollock suggests a pattern

of considerable geographic stock structure in walleye pollock. Phenotypic

differences between stocks, elemental composition of otoliths, and parasite

studies indicate restricted mixing of juveniles and adults. Genetic differences

appear between broad regions, but resolution between adjacent stocks, especially within the eastern Bering sea, is currently lacking. All of the genetic

studies to date indicate a varying degree of genetic differentiation between

pollock in the Gulf of Alaska and Bering Sea. The potential for gene flow

during larval drift is high between adjacent stocks. However, since there

appears to be an unresolved degree of structuring within the Bering Sea, reduced gene flow due to larval retention mechanisms or strong natal homing

and philopatry is indicated.

The standard metapopulation models of Harrison (1991; Fig. 2.2) do not

fit the apparent population structure of pollock as known to date. A strawman metapopulation structure can be proposed that represents an intermediate model. This metapopulation model of pollock is made of several large

populations separated by long distances and geographical barriers (such as

the eastern Bering Sea and Sea of Okhotsk populations) with little gene flow

between them, and numerous smaller populations with potential linkages

among each other and the larger populations (Fig. 2.22). Some populations

may show local adaptations to their specific habitat, minimizing gene flow

through reliance on larval retention features and natal homing.

In spite of the importance of this resource, and the importance of stock

structure to its management, we don’t have a comprehensive genetic sur-
44 S.A. Macklin (ed.)

Figure 2.22: Hypothetical nondimensional pictogram representing the population structure of walleye pollock. Closed ellipses represent habitat patches; filled = occupied, unfilled = vacant. Dashed lines indicate

boundaries of populations. Arrows indicate relative gene flow through migration or larval transport. Probable main populations for pollock are Sea of Okhotsk and eastern Bering Sea shelf.
Bering Sea FOCI Final Report 45

vey across the whole range using modern genetic techniques. Nor is there

a finescale genetic survey, within a region where different stocks have been

identified. Such a survey would need to be adequate to determine if there

are clines that represent differences by distance, or a sudden transition representing a barrier. Many of the smaller fjord populations represent an

opportunity to examine founder effects on genetic differentiation within the

pollock metapopulation. However, these populations have not been included

in past genetic surveys. Future work should concentrate on genetic structures with high mutation rates, such as microsatellites, capable of resolving

genetic structure that may have evolved recently. Stock mixing problems can

be better addressed using these techniques in conjunction with applied tags

and natural environmental tags, such as elemental composition of otoliths.

2.5 Management Implications

The question of whether fisheries fluctuations result from local populations

waxing and waning independently or movements among populations has

been a central issue in fisheries since the time of Hjort (1914). Since that

time, most fisheries research has assumed that local populations are closed

and homogeneous systems. However, many scientists are currently suggesting that we re-examine the large-scale patterns underlying the dynamics of

fish populations (Frank, 1992). For example, prior to the collapse of the

northern cod population in the Northwest Atlantic Ocean it was believed

that there was no genetically based population structure due to extensive

egg and larval drift, followed by opportunistic and nonphilopatric recruitment of juveniles to adult assemblages (deYoung and Rose, 1993). Studies

of allozymes and mtDNA studies had little success in discriminating among

Northwest Atlantic cod stocks. However, Bentzen et al. (1996) examined

nuclear DNA microsatellite distributions and found that the northern cod

population does not represent a single panmictic assemblage, but is comprised of genetically distinguishable subunits, each of which is affiliated with

a distinct spawning area. It is of great interest that considerable finestructure has been found in Atlantic cod populations, because cod and pollock

have taxonomic as well as life history similarities.

There are several issues especially relevant to pollock stocks when genetically or geographically discrete subpopulations are lumped as single management units. Daan (1991) indicates that if catch-at-age analysis is applied to

a heterogeneous unit stock (a metapopulation), then fishing effort is underestimated and fishing mortality deviates from the recent true trend, leading

to the possibility of overfishing. Pawson and Jennings (1996) indicated that

lumping of stocks may lead to reductions in short-term yields. The depletion

of unidentified local subpopulations and their possible extinction is another

issue (Ovenden, 1990). The rate of recovery of geographically but not genetically discrete populations will depend on the level of gene flow between

subpopulations. Genetically distinct subpopulations, by definition, have low

levels of gene flow among them, and specific stock adaptations to local habitat conditions can impede recovery from extrinsic source populations.

There are some other key areas where high-resolution stock identification
46 S.A. Macklin (ed.)

would be extremely useful in management of pollock harvests. A central issue

in the case of pollock management is whether broad-scale migrations occur

that result in seasonal mixing of subpopulations. For example, if eastern

or western Bering Sea fish migrate across or around the Basin (as believed

by Dawson, 1994), they may be harvested on both sides of the Bering Sea

basin. Therefore, a migratory population would experience two independent

sources of fishing mortality in two management regions.

Recently, new local populations of pollock have been discovered. Whether

they will be maintained as self-sustaining populations or whether they are

ephemeral stocks is a question that depends upon the mechanism of natal

spawning and local adaptation for reproductive success. For example, in

recent years a spawning population of 300,000 tons has been found around

the Shumagin Islands in the western Gulf of Alaska (C. Wilson, Alaska Fisheries Science Center, 7600 Sand Point Way NE, Seattle, WA 98115, personal

communication, October 1996). This population is largely composed of the

1989 year class, which was strong in the Bering Sea, but weak in the rest of

the Gulf of Alaska. It is unknown whether this population originated from

density-dependent dispersal from the Bering Sea, or whether it represents an

increase in a previously unknown local subpopulation. Another explanation

may be that vagrants from the Bering Sea could have joined a small local

spawning population.

Research on spawner-recruitment relationships is also dependent on the

definition of stock structure among populations. For example, consider the

following hypothetical but realistic example: if two genetically distinct and

asynchronously fluctuating populations, A and B, are lumped together in a

VPA analysis, dominance shifts could result in a spawner-recruit relationship where recruits from population A are compared to egg production from

population B. Shifts in dominance between putative stocks appears to be a

situation particularly applicable to pollock in the Bering Sea (Francis and

Bailey, 1983). In this case, knowledge of the underlying population structure would vastly improve the understanding of spawner-recruit relationships. Alternatively, different spatial scales can be a problem when early life

dynamics in the juvenile nursery of population A are compared to recruits

derived from VPA analysis of lumped populations; this type of comparison

is common in fisheries research. Other confounding cases may occur where

there is vagrancy of recruits or an exogenous source of recruits, such as might

occur with pollock in the Gulf of Alaska. All of these circumstances can result in misinterpretations of the factors underlying the dynamics of these

populations.

The mechanism of natal-site fidelity has broad implications to fisheries

management and sustainable harvesting of these populations. For example,

if fish learn their migration routes from older fish, currently thought to be

important for cod (Rose, 1993) and herring (Corten, 1993), then removing

older fish from the population can lead to increased straying of younger fish

due to loss of social tradition. Furthermore, this mechanism implies that

larvae dispersed from the range of adults can adopt new local populations.

The mechanism of “innate” or “genetic memory” implies that removal of

any fish is of equal importance to the population, but it is essential not
Bering Sea FOCI Final Report 47

to drive a population into extinction, because recolonization will depend on

the process of natural selection and adaptation to local conditions. Vagrants

from other populations are unlikely to spawn with local populations in the

same region. Imprinting implies that harvesting will not have an impact

on migratory routes, and heavily depleted populations can be re-seeded. In

fact, marine fish species probably use a combination of all of these mechanisms for natal fidelity, and the response to any one stimulus is graded

against others. It is not known which homing mechanisms are utilized by

pollock during spawning migrations; however, the existence of genetic structure in the population, which is maintained in spite of larval drift and highly

dispersed feeding migrations, tends to indicate a genetic-based mechanism.

Based on the complex range of behaviors pollock are capable of exhibiting

(Olla et al., 1996) it should not be surprising that they show considerable

flexibility in their homing behavior.

New paradigms for managing fisheries in a sustainable manner are urgently needed, and these concepts are largely dependent upon better definition of stock distributions and interrelationships. In a review of stock structure methods, Pawson and Jennings (1996) suggest that despite widespread

application of genetic techniques, there are only a few cases where these studies have provided information to managers that could have been adopted,

except for salmon. Certainly, information indicating multiple genetic-based

stocks adds another element of concern to fisheries managers and makes their

task more complex (Lincoln, 1994). As noted by Carvalho and Hauser (1994)

good communication between fisheries managers and geneticists is needed for

effective implementation of stock structure information, including clear objectives for proposed work and utilization of appropriate techniques. Future

work on stock structure of walleye pollock should be closely coordinated with

scientists responsible for establishing pollock harvest policies.

Given the high potential for gene flow in marine species including pollock, genetic approaches alone may not completely resolve stock structure

issues at the level of harvest stocks or ecological populations; tagging studies

offer another way to study linkages between fish populations. Gauldie (1991)

suggests that tagging studies and monitoring catch statistics are methods to

assess how much fishing in one place/time affects groups of fishes in other

places (harvest stocks). Pawson and Jennings (1996) are also proponents

of tagging studies for providing evidence of stock separation and migration,

and indicate that carefully planned tagging experiments, or experiments utilizing naturally acquired tags, are needed to establish a relationship between

fishes in different regions. Although not necessarily showing levels of gene

flow between areas, well thought out and executed tagging and/or transplant experiments would offer a powerful approach to studying migration

mechanisms. Tagging pollock has been problematic in the past due to issues of barotrauma, tag recovery bias, and distribution of effort, and the

large number of tags necessary to characterize such large populations. New

technologies should be developed to minimize these problems, including environmental tags, such as otolith chemical fingerprints, and in situ tagging.

Studies of fish dispersal that are coordinated with modern genetic studies
48 S.A. Macklin (ed.)

should contribute significantly to understanding linkages between population

dynamics and structure of marine fish populations.

2.6 Acknowledgments

Arthur Kendall, Paul Bentzen, Carol Sibley, Robin Waples, Stew Grant, Ric

Brodeur, Phyllis Stabeno, and Mike Canino reviewed sections, or in some cases all of

an earlier version of this manuscript. I also thank Dennis Powers, Phyllis Stabeno,

Steven Porter, Annette Brown, Akira Nishimura, Jim Traynor, Gary Villa, Joseph

Quattro, Allen Macklin, and Susan Picquelle for contributing information used in

this report.

2.7 References

Andrewartha, H.G., and L.C. Birch (1954): The Distribution and Abundance of

Animals. University of Chicago Press, Chicago.

Arthur, J.R. (1983): A preliminary analysis of the discreteness of stocks of walleye pollock, Theragra chalcogramma, from the northeastern Pacific Ocean off

Canada based on their parasites. Can. Tech. Rep. Fish. Aquat. Sci., 1184, 15

pp.

Avdeev, V.V., and G.V. Avdeev (1989): A study of walleye pollock population

structure and migration routes using parasitological indicators. In Proceedings

of the International Symposium on the Biology and Management of Walleye

Pollock, Alaska Sea Grant Rept. No. 89-1, University of Alaska, Fairbanks,

569–590.

Avise, J.C. (1994): Molecular Markers, Natural History and Evolution. Chapman

and Hall, NY.

Bailey, K.M. (1989): Interaction between the vertical distribution of juvenile walleye

pollock Theragra chalcogramma in the eastern Bering Sea, and cannibalism.

Mar. Ecol. Prog. Ser., 53, 205–213.

Bailey, K.M., R.D. Brodeur, and A.B. Hollowed (1996a): Cohort survival patterns

of walleye pollock, Theragra chalcogramma, in Shelikof Strait, Alaska: A critical

factor approach. Fish. Oceanogr., 5, 179–188.

Bailey, K.M., S.J. Picquelle, and S.M. Spring (1996b): Mortality of larval walleye

pollock Theragra chalcogramma in the western Gulf of Alaska, 1988–91. Fish.

Oceanogr., 5, 124–136.

Bailey, K.M., M.F. Canino, J.M. Napp, S.M. Spring, and A.L. Brown (1995): Contrasting years of prey levels, feeding conditions and mortality of larval walleye

pollock Theragra chalcogramma in the western Gulf of Alaska. Mar. Ecol. Prog.

Ser., 119, 11–23.

Bailey, K.M., and S.A. Macklin (1994): Analysis of patterns in larval walleye pollock

Theragra chalcogramma survival and wind mixing events in Shelikof Strait, Gulf

of Alaska. Mar. Ecol. Prog. Ser., 113, 1–13.

Bakkala, R.G. (1993): Structure and historical changes in the groundfish complex

of the eastern Bering Sea. NOAA Tech. Rept. NMFS-114, 91 pp.

Bentzen, P., C.T. Taggart, D.E. Ruzzante, and D. Cook (1997): Microsatellite

polymorphism and the population structure of Atlantic cod (Gadus morhua) in

the northwest Atlantic. Can. J. Fish. Aquat. Sci., 53, 2706–2721.

Bernatchez, L., and S. Martin (1996): Mitochondrial DNA diversity in anadromous

rainbow smelt, Osmerus mordax Mitchill: A genetic assessment of the membervagrant hypothesis. Can. J. Fish. Aquat. Sci., 53, 424–433.

Bograd, S.J., P.J. Stabeno, and J.D. Schumacher (1994): A census of mesoscale

eddies in Shelikof Strait, Alaska, during 1989. J. Geophys. Res., 99, 18,243–

18,254.
Bering Sea FOCI Final Report 49

Boorman, S.A., and P.R. Levitt (1973): Group selection on the boundary of a stable

population. Theor. Pop. Biol., 4, 85–128.

Brown, J.H. (1984): On the relationship between abundance and distribution of

species. American Naturalist, 123, 253–279.

Brown, J.H. (1995): Macroecology. Univ. Chicago Press, Chicago.

Canino, M.F., K.M. Bailey, and L.S. Incze (1991): Temporal and geographic differences in feeding and nutritional condition of walleye pollock larvae Theragra

chalcogramma in Shelikof Strait, Gulf of Alaska. Mar. Ecol. Prog. Ser., 79,

27–35.

Carr, S.M., A.J. Snellen, K.A. Howse, and J.S. Wroblewski (1995): Mitochondrial

DNA sequence variation and the genetic stock structure of Atlantic cod (Gadus

morhua) from bay and off shore locations on the Newfoundland continental

shelf. Mol. Ecol., 4, 79–88.

Carvalho, G.R., and L. Hauser (1994): Molecular genetics and the stock concept in

fisheries. Rev. Fish. Biol. Fisheries, 4, 326–350.

Corten, A. (1993): Learning processes in herring migrations. ICES C.M. 1993/H:18.

Daan, N. (1991): Bias in virtual population analysis when the unit stock assessed

consists of sub-stocks. ICES C.M. 1991/D:17.

Dawson, P. (1994): The stock structure of Bering Sea walleye pollock (Theragra

chalcogramma). Master of Science Thesis, University of Washington, Seattle,

220 pp.

Dell’Arciprete, O.P. (1992): Growth, mortality, and transport of walleye pollock

larvae (Theragra chalcogramma) in the eastern Bering Sea. Master of Science

Thesis, University of Washington, Seattle, 105 pp.

deYoung, B., and G.A. Rose (1993): On the recruitment and distribution of Atlantic

cod (Gadus morhua) off Newfoundland. Can. J. Fish. Aquat. Sci., 50, 2729–

2741.

Doherty, P.J., S. Planes, and P. Mather (1995): Gene flow and larval duration in

seven species of fish from the Great Barrier Reef. Ecology, 76, 2373–2391.

Efremov, V.V., E.V. Mikhajlova, and V.B. Molokanov (1989): Aconitase, a new

and promising marker to be used in genetic studies of Theragra chalcogramma

populations. Genetika, 25, 2263–2265 (English abstract only).

Francis, R.C., and K.B. Bailey (1983): Factors affecting recruitment of selected

gadoids in the northeast Pacific and east Bering Sea. In From Year to Year,

W. Wooster (ed.), Washington Sea Grant, University of Washington, Seattle,

35–60.

Frank, K.T. (1992): Demographic consequences of age-specific dispersal in marine

fish populations. Can. J. Fish. Aquat. Sci., 49, 2222–2231.

Garc ́ıa de Le ́on, L. Chikhi, and F. Bonhomme (1997): Microsatellite polymorphism

and population subdivision in natural populations of European sea bass Dicentrarchus labrax (Linnaeus, 1758). Mol. Ecol., 6, 51–62.

Gauldie, R.W. (1991): Taking stock of genetic concepts in fisheries management.

Can. J. Fish. Aquat. Sci., 48, 722–731.

Gonzalez-Villasenor, L.I., and D.A. Powers (1990): Mitochondrial DNA restriction site polymorphisms in the teleost Fundulus heteroclitus support secondary

intergradation. Evolution, 44, 27-37.

Gong, Y., Y.H. Hur, and S.S. Kim (1990): Comparison of meristic characters of

Alaska pollock, Theragra chalcogramma, from seven geographic areas of the

North Pacific. In Compilation of Papers Presented at the International Symposium on Bering Sea Fisheries. Alaska Fisheries Science Center, Seattle, WA,

77–82.

Grant, W.S., and F.M. Utter (1980): Biochemical genetic variation in walleye pollock Theragra chalcogramma: population structure in the southeastern Bering

Sea and Gulf of Alaska. Can. J. Fish. Aquat. Sci., 37, 1093–1100.
50 S.A. Macklin (ed.)

Hanski, I., and M. Gilpin (1991): Metapopulation dynamics: Brief history and

conceptual domain. In Metapopulation Dynamics, M. Gilpin and I. Hanski

(eds.), Academic Press, Inc., San Diego, CA, 3–16.

Harrison, S. (1991): Local extinction in a metapopulation context: An empirical

evaluation. In Metapopulation Dynamics, M. Gilpin and I. Hanski (eds.), Academic Press, Inc., San Diego, CA, 73–88.

Hashimoto, R., and S. Koyachi (1969): Biology of the Alaska pollock, Theragra

chalcogramma (Pallas), distributed on the fishery grounds of the Tohoku districts and the Pacific coast of Hokkaido, southward from the Erimo ground, I,

The morphological differentiation of the three types and the comparison with

the other fishery ground’s groups. Bull. Tohoku Reg. Fish. Res. Lab., 29, 37–92

(in Japanese with English summary).

Hashimoto, R., and S. Koyachi (1977): Geographical variation of relative growth of

walleye pollack Theragra chalcogramma (Pallas). Bull. Tohoku Reg. Fish. Res.

Lab., 38, 41–74 (in Japanese with English summary).

Hedgecock, D. (1994): Temporal and spatial genetic structure of marine animal

populations in the California Current. CalCOFI Rept., 35, 73–81.

Hillgruber, N., L.J. Haldorson, and A.J. Paul (1995): Feeding selectivity of larval

walleye pollock Theragra chalcogramma in the oceanic domain of the Bering

Sea. Mar. Ecol. Prog. Ser., 120, 1–10.

Hinckley, S. (1987): The reproductive biology of walleye pollock, Theragra chalcogramma, in the Bering Sea, with reference to spawning stock structure. Fish.

Bull. U.S., 85(3), 481–498.

Hinckley, S., K.M. Bailey, S. Picquelle, J.D. Schumacher, and P.J. Stabeno (1991):

Transport, distribution and abundance of larval and juvenile walleye pollock

(Theragra chalcogramma) in the western Gulf of Alaska. Can. J. Fish. Aquat.

Sci., 48, 91–98.

Hjort, J. (1914): Fluctuations in the great fisheries of northern Europe. Rapp.

Proc. Verb. Cons. Int. Explor. Mer, 20, 1–228.

Ishida, T. (1954): On the age determination and morphometrical differences of the

otolith of Alaska pollock in the Hokkaido coast. Bull. Hokkaido Reg. Fish. Res.

Lab., 11, 36–67 (in Japanese with English summary).

Iwata, M. (1973): Genetic polymorphism of tetrazolium oxidase in walleye pollock.

Jpn. J. Genet., 48, 147–149.

Iwata, M. (1975a): Population identification of walleye pollock, Theragra chalcogramma (Pallas), population in the vicinity of Japan. Memo. Fac. Fish. Hokkaido

Univ., 22, 193–258.

Iwata, M. (1975b): Genetic identification of walleye pollock, Theragra chalcogramma (Pallas), populations on the basis of tetrazolium oxidase polymorphism.

Comp. Biochem. Physiol., 50B, 197–201.

Iwata, M., and I. Hamai (1972): Local forms of walleye pollock, Theragra chalcogramma (Pallas) classified by number of vertebrae. Bull. Jpn. Soc. Sci. Fish.,

38(10), 1129–1142.

Janusz, J. (1994): How many pollock (Theragra chalcogramma) stocks support the

fishery in the Sea of Okhotsk. Bull. Sea Fish. Inst. Gdynia, 132, 67–68(English

abstract).

Janusz, J., T.B. Linkowski, and M. Kowalewska-Pahlke (1989): Results of the population studies of walleye pollock Theragra chalcogramma in the Bering Sea. In

Proceedings of the International Scientific Symposium on Bering Sea Fisheries,

NOAA Tech. Memo. NMFS F/NWC-163, Alaska Fisheries Science Center, Seattle, WA, 216–230.

Jarne, P., and P.J.L. Logoda (1996): Microsatellites, from molecules to populations

and back. Trends Ecol. Evol., 11, 424–429.
Bering Sea FOCI Final Report 51

Johnson, A.G. (1977): A survey of biochemical variants found in groundfish stocks

from the North Pacific and Bering Sea. Anim. Blood Groups Biochem. Genet.,

8, 13–19.

Kendall, A.W., J.D. Schumacher, and S. Kim (1996): Walleye pollock recruitment

in Shelikof Strait: Applied fisheries oceanography. Fish. Oceanogr., 5, 4–18.

Kennedy, P.K., M.L. Kennedy, E.G. Zimmerman, R.K. Chester, and M.H. Smith

(1986): Biochemical genetics of mosquito fish, V, Perturbation effects on genetic

organization of populations. Copeia, 1986, 937–945.

Kim, S., and A.W. Kendall, Jr. (1989): Distribution and transport of larval walleye

pollock (Theragra chalcogramma) in Shelikof Strait, Gulf of Alaska, in relation

to water movement. Rapp. P.-v. Reun. Cons. Int. Explor. Mer, 191, 127–136.

Koyachi, S., and R. Hashimoto (1977): Preliminary survey of variations of meristic

characteristics of walleye pollock Theragra chalcogramma (Pallas). Bull. Tohoku

Reg. Fish. Res. Lab., 38, 17–40 (in Japanese with English summary).

Lawton, J.H., S. Nee, A.J. Letcher, and P.H. Harvey (1994): Animal distributions:

Patterns and processes. In Large-Scale Ecology and Conservation, P.J. Edwards,

R.M. May, and N.R. Webb (eds.), Blackwell Sci. Publ., Oxford, 41–58.

Levins, R. (1970): Extinction. In Some Mathematical Problems in Biology, M.

Gersternhaber (ed.), American Mathematical Society, Providence, RI, 77–107.

Lincoln, R. (1994): Molecular genetics applications in fisheries: Snake oil or restorative? Rev. Fish. Biol. Fish., 4, 389–392.

Lynde, C.M., M.V.H. Lynde, and R.C. Francis (1986): Regional and temporal

differences in growth of walleye pollock (Theragra chalcogramma) in the eastern

Bering Sea and Aleutian Basin with implications for management. Unpublished

manuscript, 48pp., Northwest and Alaska Fish. Cent., Natl. Mar. Fish. Serv.,

NOAA, 7600 Sand Point Way NE, Seattle, WA 98115.

MacArthur, R.H., and E.O. Wilson (1967): The Theory of Island Biogeography.

Princeton University Press, Princeton, N.J., 203 pp.

McConnaughey, R.A. (1995): Changes in geographic dispersion of eastern Bering

Sea flatfish associated with changes in population size. In Proceedings of the

International Symposium on North Pacific Flatfish, Alaska Sea Grant Program,

Fairbanks, 385–406.

Matthews, K.R. (1990): An experimental study of the habitat preferences and

movement patterns of copper, quillback, and brown rockfishes (Sebastes spp.).

Env. Biol. Fish., 29, 161–178.

Mulligan, T.J., K.M. Bailey, and S. Hinckley (1989): The occurrence of larval and

juvenile walleye pollock, Theragra chalcogramma, in the eastern Bering Sea with

implications for stock structure. In Proceedings of the International Symposium

on the Biology and Management of Walleye Pollock, Alaska Sea Grant Rept.

No 89-1, University of Alaska, Fairbanks, 471–490.

Mulligan, T.J., R.W. Chapman, and B.L. Brown (1992): Mitochondrial DNA analysis of walleye pollock, Theragra chalcogramma, from the eastern Bering Sea

and Shelikof Strait, Gulf of Alaska. Can. J. Fish. Aquat. Sci., 49, 319–326.

Nakano, H., M. Takahashi, and K. Kikuchi (1991): Geographical differences of

walleye pollock caught from three Bering Sea areas from standpoint of metal

and amino acid contents of otoliths. Int. Pac. Fish. Comm. Doc. 3668, Fisheries

Agency of Japan, National Res. Inst. of Far Sea Fisheries, 7-1 Orido 5 chome,

Shimizu, Shizuoka, Japan 424, 14 pp.

Napp, J.M., L.S. Incze, P.B. Ortner, D.L.W. Siefert, and L. Britt (1996): The plankton of Shelikof Strait, Alaska: Standing stock, production, mesoscale variability

and their relevance to larval fish survival. Fish. Oceanogr., 5, 19–38.

National Research Council (1996): The Bering Sea Ecosystem. National Academy

Press, Wash., D.C. 307 pp.
52 S.A. Macklin (ed.)

Nitta, A., and T. Sasaki (1990): Study of stock identification of walleye pollock

based on morphometric data. In Compilation of Papers Presented at the International Symposium on Bering Sea Fisheries, Alaska Fisheries Science Center,

Seattle, WA, 74–76.

Ogata, T. (1959): Population studies of the Alaska pollock in the Sea of Japan, I,

On the variation in the vertebral count. Ann. Rept. Jap. Sea Reg. Fish. Res.

Lab., 5, 119–125 (in Japanese with English summary).

Olla, B.L., M.W. Davis, C.H. Ryer, and S.M. Sogard (1996): Behavioral determinants of distribution and survival in early stages of walleye pollock, Theragra

chalcogramma: a synthesis of experimental studies. Fish. Oceanogr., 5, 167–178.

Ovenden, J.R. (1990): Mitochondrial DNA and marine stock assessment: A review.

Aust. J. Mar. Freshwater Res., 41, 835–853.

Palsson, W.A., K. Hoeman, G.G. Bargmann, and D. Day (1996): Draft report,

Puget Sound bottomfish status of stocks. Wash. Dept. Fish.

Pawson, M.G., and S. Jennings (1996): A critique of methods for stock identification

in marine capture fisheries. Fish. Res., 25, 203–217.

Powers, D.A. (1996): The use of molecular techniques to dissect the genetic architecture of pollock populations. Report to the Coastal Ocean Program.

Quinn, T.P. (1993): A review of homing and straying of wild and hatchery-produced

salmon. Fish. Res., 18, 29–44.

Quinn, T.P., and R.D. Brodeur (1991): Intra-specific variations in the movement

patterns of marine animals. Amer. Zool., 31, 231–241.

Rand, D.M. (1996): Neutrality test of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Cons. Biol.,

10, 665–671.

Rose, G.A. (1993): Cod spawning on a migration highway in the north-west Atlantic. Nature, 366, 458–461.

Ruzzante, D.E., C.T. Taggart, D. Cook, and S. Goddard (1996a): Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua L.) off

Newfoundland: Microsatellite DNA variation and antifreeze level. Can. J. Fish.

Aquat. Sci., 53, 634–645.

Ruzzante, D.E., C.T. Taggart, and D. Cook (1996b): Spatial and temporal variation

in the genetic composition of a larval cod (Gadus morhua) aggregation: Cohort

contribution and genetic stability. Can. J. Fish. Aquat. Sci., 53, 2695–2705.

Saunders, M.W., G.A. McFarlane, and W. Shaw (1989): Delineation of walleye

pollock (Theragra chalcogramma) stocks off the Pacific coast of Canada. In

Proceedings of the International Symposium on the Biology and Management

of Walleye Pollock, Alaska Sea Grant Rept. No. 89-1, University of Alaska,

Fairbanks, 379–401.

Serobaba, I.I. (1977): Data on the population structure of the walleye pollock,

Theragra chalcogramma (Pallas), from the Bering Sea. Vopr. Ikhtiol., 17, 247–

260 (in Russian) (English translation 1978, J. Ichthyol., 17, 219–231).

Severin, K.P., J. Carroll, and B.L. Norcross (1995): Electron microprobe analysis of

juvenile walleye pollock, Theragra chalcogramma, otoliths from Alaska: A pilot

stock separation study. Env. Biol. Fish., 43, 269–283.

Schumacher, J.D., and A.W. Kendall, Jr. (1995): An example of fisheries oceanography: Walleye pollock in Alaskan waters. Rev. Geophys. (suppl.), 1153–1163.

Schumacher, J.D., P.J. Stabeno, and S.J. Bograd (1993): Characteristics of an eddy

over a continental shelf: Shelikof Strait, Alaska. J. Geophys. Res., 98, 8395–

8404.

Schumacher, J.D., and P.J. Stabeno (1994): Ubiquitous eddies of the eastern Bering

Sea and their coincidence with concentrations of larval pollock. Fish. Oceanogr.,

3, 182–190.
Bering Sea FOCI Final Report 53

Schumacher, J.D., and P.J. Stabeno (1997): The continental shelf of the Bering

Sea. In The Sea, Vol. 10 (in press).

Shaw, W., and G.A. McFarlane (1986): Biology, distribution and abundance of

walleye pollock (Theragra chalcogramma) off the west coast of Canada. Int.

North Pac. Fish. Comm. Bull., 45, 262–283.

Shields, G.F., and J.R. Gust (1995): Lack of geographic structure in mitochondrial

DNA sequences of Bering Sea walleye pollock, Theragra chalcogramma. Mol.

Mar. Biol. Biotech., 4, 69–82.

Sinclair, M. (1988): Marine populations: An essay on population regulation and

speciation. Washington Sea Grant Press, Seattle.

Slatkin, M. (1987): Gene flow and the geographical structure of natural populations.

Science, 236, 787–792.

Smith, P.J., A. Jamieson, and A.J. Birley (1990): Electrophoretic studies and the

stock concept in marine teleosts. J. Cons. Int. Explor. Mer, 47, 231–245.

Somerton, D. (1978): Competitive interaction of walleye pollock and Pacific Ocean

perch in the northern Gulf of Alaska (abstract). In Fish Food Habit Studies,

S.J. Lipovsky, and C.A. Simenstad (ed.), Washington Sea Grant, University of

Washington, Seattle, 163.

Sogard, S.M., and B.L. Olla (1996): Food deprivation affects vertical distribution

and activity of a marine fish in a thermal gradient: Potential energy-conserving

mechanisms. Mar. Ecol. Prog. Ser., 133, 43–55.

Stabeno, P.J., R.K. Reed, and J.D. Schumacher (1995): The Alaska coastal current:

Continuity of transport and forcing. J. Geophys. Res., 100(C2), 2477–2485.

Stepanenko, M.A. (1997): Variations from year to year in the spatial differentiation

of the walleye pollock, Theragra chalcogramma, and the cod, Gadus macrocephalus, in the Bering Sea. J. Ichthyol., 37, 14–20.

Svetovidov, A.N. (1948): Fauna of USSR fishes. Gadiformes, 9(4). Moscow, Zool.

Inst. Acad. Sci. USSR, 304 pp.

Swain, D.P., and E.J. Wade (1993): Density-dependent geographic distribution of

Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence. Can. J.

Fish. Aquat. Sci., 50, 725–733.

Swain, D.P., and R. Morin (1996): Relationship between geographic distribution

and abundance of American plaice (Hippoglossoides platessoides) in the southern

Gulf of St. Lawrence. Can. J. Fish. Aquat. Sci., 53, 106–119.

Swartzman, G., W. Stuetzle, K. Kulman, and M. Powojowski (1994): Relating the

distribution of pollock schools in the Bering Sea to environmental factors. ICES

J. Mar. Sci., 51, 481–492.

Taylor, A.D. (1991a): Studying metapopulation effects in predator-prey systems.

In Metapopulation Dynamics, M. Gilpin and I. Hanski (eds.), Academic Press,

Inc., San Diego, CA, 305–323.

Taylor, B. (1991b): Investigating species incidence over habitat fragments of different areas—a look at error estimation. In Metapopulation Dynamics, M. Gilpin

and I. Hanski (eds.), Academic Press, Inc., San Diego, CA, 177–191.

Temnykh, O.S. (1991): The population structure of Alaska pollock in the Okhotsk

Sea. Rybn. Khoz., 6, 28–31 (English abstract only).

Temnykh, O.S. (1994): Morphological differentiation of Alaskan pollock, Theragra

chalcogramma, in the west Bering Sea and Pacific waters of Kamchatka. J.

Ichthyol., 34, 204–211.

Theilacker, G.H., K.M. Bailey, M.F. Canino, and S.M. Porter (1996): Variations in

larval walleye pollock feeding and conditions: A synthesis. Fish. Oceanogr., 5,

112–123.

Thompson, J.M. (1981): Preliminary report on the population biology and fishery

of walleye pollock (Theragra chalcogramma) off the Pacific coast of Canada.

Can. Tech. Rep. Fish. Aquat. Sci., 1031, 157 pp.
54 S.A. Macklin (ed.)

Tsuji, S. (1989): Alaska pollock population, Theragra chalcogramma, of Japan and

its adjacent waters, I, Japanese fisheries and population studies. Mar. Behav.

Physiol., 15, 147–205.

Vastano, A.C., L.S. Incze, and J.D. Schumacher (1992): Observation and analysis

of fishery processes: Larval pollock at Shelikof Strait. Alaska. Fish. Oceanogr.,

1, 20–31.

Waples, R.S. (1987): A multispecies approach to the analysis of gene flow in marine

shore fishes. Evolution, 41, 385–400.

Wespestad, V.G. (1996): Trends in North Pacific pollock and cod fisheries. In Norfish ‘96, 15–16 August 1996, Trondheim, Norway (see http://www.afsc.noaa.

gov/refm/norfish/norfish.htm).

Wilimovsky, N.J., A. Peden, and J. Peppar (1967): Systematics of six demersal

fishes of the North Pacific Ocean. Fish. Res. Board Can. Tech. Rep., 34, 95 pp.

Wright, J.M., and P. Bentzen (1994): Microsatellites: Genetic markers for the

future. Rev. Fish. Biol. Fisheries, 4, 384–388.
Bering Sea FOCI Final Report 55

Part 2A

The use of molecular techniques to dissect the

genetic architecture of pollock populations

(Dennis A. Powers1)

One of the main goals of fisheries biologists is to understand the mechanisms

that regulate the distribution and abundance of marine fish. Elucidation of

these mechanisms requires an understanding of the genetic architecture of

the fish species, including the ability to discriminate between stocks and determine the relative contributions of these stocks to the fishery. During the

initial phase of our project, we developed pollock-specific polymerase chain

reaction (PCR) methods to test the hypothesis that “there are distinct Pollock stocks in the Bering Sea.” After these methods were developed, we

analyzed 164 individual pollock samples that represented populations sampled from the Gulf of Alaska, Bering Sea, and Sea of Japan. Using 47 individuals as population representatives, we initially sequenced 300 base pairs

of DNA for each of two mitochondrial genes (i.e., cytochrome-b and ATPase) for each individual fish. Our sequencing results identified 14 mtDNA

haplotypes, three of which were in high enough frequency to be informative

for tests of population subdivision. These three haplotypes were defined by

base substitutions at two different DNA sequence sites: Haplotype 3 – AA;

Haplotype 7 – GA, and Haplotype 13 – GG.

Forty-seven individuals were sequenced for approximately 600 base pairs;

300 base pairs each for cytochrome-b and ATPase. Individuals represented

all populations sampled from the Gulf of Alaska, Bering Sea, and Sea of

Japan. Fourteen mtDNA haplotypes were found, three of which were in

high enough frequency to be informative for tests of population subdivision.

These three haplotypes were defined by base substitutions at two sites.

Haplotype 3 – AA

Haplotype 7 – GA

Haplotype 13 – GG

where the first position is found in cytochrome-b, and the second in ATPase8. Substitutions at both sites were silent, the first a third-position substitution in a threonine codon, the second a third-position substitution in a

glutamic acid codon. A restriction enzyme assay was developed to score 117

additional individuals for these three haplotypes (a total of 164 individuals)

(Table 2A.1).

An analysis of molecular variance (AMOVA) was performed on the aggregate data (164 individuals) representing nine populations. Most of the

variation was found to be within populations (85.5%), although a small but

significant proportion was among populations (14.5%). A UPGMA den1Hopkins Marine Station, Stanford University, Pacific Grove, CA 93940, U.S.A.
56 S.A. Macklin (ed.)

Table 2A.1: Cytochrome-b and ATPase-8haplotypes from different areas of the Bering Sea.

Haplotype Pairs

AA GO GA

America

Northeastern Shelf 4 12 4

Aleutian Basin 6 7 3

Southeastern Aleutian 6 11 2

Northeastern Aleutian 3 9 2

Gulf of Alaska 3 20 5

Southeastern Shelf 8 11 1

Asia

East Kamchatka 3 6 12

West Bering Sea 4 9 10

Sea of Japan 0 1 2

Table 2A.2: Tests for temporal variation.

Locality Years Compared Probability Significance

Gulf of Alaska 1988 vs 1994 0.3866 ns

Southeast Shelf 1988 vs 1991 0.1648 ns

Northeast Aleutians 1988 vs 1991 0.9021 ns

drogram (Fig. 2A.1) using among-population genetic distances revealed evidence for a distinct split between American (Gulf of Alaska and Eastern

Bering Sea) and Asian (Sea of Japan and Western Bering Sea) populations,

primarily in the distribution of the GG and GA haplotypes. An AMOVA

revealed that haplotype frequencies within each group differed significantly

(P < 0.0002). An analysis of these data using the Neighbor Joining Method

was consistent with the distinct division between American and Asian populations. As was the case for the dendogram derived by the DA genetic

distance analysis (Fig. 2A.2), the Neighbor Joining Method also revealed

considerable substructure within the larger American and Asian clusters.

Some of the smaller clusters were consistent with the substructure derived

by the UPGM genetic distance dendogram illustrated in Fig. 2A.2, while

others were slightly different. If we could significantly expand the sample

size for each of the nine populations involved in this study and provide data

for these populations between year classes, there is a very high likelyhood

that we could discriminate between all nine populations on the basis of RFLP

analysis of mtDNA haplotypes.

Based on the DNA sequence data of these 47 individuals, we developed a

restriction enzyme assay that allowed the rapid identification of mtDNA haplotypes based on restriction fragment length polymorphisms (RFLP) using

gel electrophoresis. Employing this RFLP analysis, 117 additional individual

pollock were analyzed for the three mtDNA haplotypes identified by DNA sequence analyses. After the methods were developed, we analyzed 164 pollock

DNA samples representing nine populations from the Gulf of Alaska, Bering
Bering Sea FOCI Final Report 57

Figure 2A.1: UPGG Dendogram utilizing the Standard Genetic Distance Method of analysis.

Figure 2A.2: UPGM Dendogram utilizing the DA-Genetic Distance Method of analysis.

Sea, and Sea of Japan. An analysis of molecular variance (AMOVA) was

performed on the aggregate data of 164 individuals representing nine populations. Most of the variation was found to be within populations (85.5%),

although a small but significant proportion was among populations (14.5%).

In order to better define those populations, we expanded the sample size and

analyzed samples from an earlier year to determine if the greater variation

within populations was the result of pooling samples collected from different year classes. We developed the following specific goals for October 1995

through September 30, 1996 in order to attack this problem:

(i) analyze samples collected from populations in 1988,

(ii) analyze new samples collected from nine populations in 1994,

(iii) compare the results of the 1988 and 1994 samples with those collected

and analyzed early,
58 S.A. Macklin (ed.)

Figure 2A.3: UPGMA dendrogram of Bering Sea and Gulf of Alaska walleye pollock, based on genetic

distances at the microsatellite locus Gmo-2. Number in parentheses correspond to the population numbers

on the map (Figure 4).

(iv) do an analysis of variance of the temporal and spatial data sets.

By the end of 1995 we had already made substantial progress toward

achieving these specific goals. For example, we had expanded the sample size

from 164 individuals to 262 samples. In an attempt to determine if there was

a temporal component of the data that could help explain the larger variation within populations than between populations that we reported last year,

we analyzed samples collected in 1988 from the Gulf of Alaska, the Northeast Aleutians, and the Southeast Shelf and compared them with samples

collected in 1994 and 1991 from those sites. However, tests for temporal

variation between 1988 samples and samples collected later did not identify significant differences between year classes (Table 2A.2). Consequently,

we reject the hypothesis that the larger variation that we observed within

populations was derived from temporal variation between year classes.

Since our previous report, we have identified a small proportion (i.e.,

four) of the AG haplotype. This haplotype is probably a rare convergent

change. The distribution of the haplotypes between geographical regions for

1988, 1991, and 1994 are shown in Table 2A.3.

Even though there was still greater variation within than between populations, the additional data maintained the same small but significant difference between populations that we previously reported. There remained

a sharp discrimination between Asian and American groups. However, expanding the sample size did not provide better discrimination between populations.

Since expanding the sample size of the populations did not dramatically

improve our ability to discriminate between populations, we undertook an

analysis of minisatellite elements (i.e., “DNA Fingerprinting”) of pollock

populations. However, none of the minisatellite loci screened yielded useful

information. We surveyed some of the pollock nuclear genome for variation in

the number of tandemly repeated microsatellite elements. We screened seven
Bering Sea FOCI Final Report 59

Table 2A.3: Distribution of haplotypes between geographical regions for 1988, 1997, and 1994.

Haplotype

AA GG GA AG

America

Northeastern Shelf 1991 4 12 4 0

Aleutian Basin 1991 6 7 3 0

Southeastern Aleutian 1991 6 11 2 1

Northeastern Aleutian 1988 10 23 6 1

Northeastern Aleutian 1991 3 9 2 0

Gulf of Alaska 1988 3 20 6 1

Gulf of Alaska 1994 3 20 5 0

Southeastern Shelf 1988 6 21 5 0

Southeastern Shelf 1991 4 9 10 0

Asia

East Kamchatka 1991 4 8 9 0

West Bering Sea 1991 4 9 10 0

Sea of Japan 1994 0 1 2 0

microsatellite primers for the polymerase chain reaction (PCR) that have

been previously shown to amplify regions in several gadid species (Brooker

et al., 1994). These primers were used to analyze 221 individual pollock representing seven pollock populations. Of those primers, three pairs (Gmo2,

Gmo9, Gmo145) gave detectable product, and two (Gmo2 and Gmol45)

showed genetic variation. Using the Gmo145 primer, we identified 19 detectable alleles and one allele that appeared that did not yield a PCR product (Table 2A.4).

Since there was a lack of detectable PCR product, conditions of the template DNA were tested with two universal PCR primers (ACT1 and ACT4).

Because all the individuals that did not yield a PCR product with Gmo145

primers gave detectable PCR products when amplified with the ACTI and

ACT4 primers, these data suggest that the absence of product for Gmo145

may be due to a “null allele” at this locus resulting from one or more sequence differences in the priming region of Gmo145. When the putative

“null allele” is scored as a separate allele, it is clear that the vast majority of the Asian populations have much higher frequencies than American

populations.

The microsatellite data in Table 2A.5 appears to give the same general

discrimination between Asian and American populations as was obtained by

the haplotypes described earlier in this report. Moreover, there is a suggestion for further subdivisions in Table 2A.5 but a proper statistical analysis

must be done before we can be sure if the apparent trend is significant.

The statistical analysis of haplotype and microsatellite data is one of

our major goals for the remainder of our funding period after which we will

publish the results in internationally refereed journals. For the haplotype

data, an analysis of molecular variance (AMOVA) like that performed last

year on the aggregate data (164 individuals) representing nine populations

will be done on the expanded data set. Dendograms utilizing DA genetic
60 S.A. Macklin (ed.) Table 2A.4: Alleles for Gmo 145 microsatellite locus. Alleles 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 18 Null Total NE Aleutians 1 0 3 2 5 7 0 23 6 1 0 0 0 0 0 0 0 0 0 0 48 NE Shelf 0 0 0 1 3 2 1 8 3 1 0 0 0 1 0 0 0 0 0 0 20 Aleutian Basin 0 0 1 1 6 6 0 29 4 2 1 0 0 0 0 0 0 0 0 0 50 S. Kamchatka 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 68 68 W. Bering Sea 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 34 34 Shelikof Strait 1 1 6 3 19 12 0 48 42 9 3 1 2 2 4 1 2 1 1 0 158 Table 2A.5: Frequencies of microsatellite alleles of pollock popu- lations. Alleles 1 2 3 4 5 6 7 8 9 10 11 13 14 15 16 17 18 18 Null NE Aleutians .020 .000 .063 .042 .104 .146 .000 .479 .125 .020 .000 .000 .000 .000 .000 .000 .000 .000 .000 NE Shelf .000 .000 .000 .050 .150 .100 .050 .400 .150 .050 .000 .000 .050 .000 .000 .000 .000 .000 .000 Aleutian Basin .000 .000 .020 .020 .120 .120 .000 .580 .080 .040 .020 .000 .000 .000 .000 .000 .000 .000 .000 S. Kamchatka .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 1.00 W. Bering Sea .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 .000 1.00 Shelikof Strait .006 .006 .038 .019 .120 .076 .000 .304 .266 .057 .019 .006 .013 .013 .006 .013 .006 .006 .000
Bering Sea FOCI Final Report 61 Figure 2A.4: Map of sampling sites and hypothetical schematic showing routes of gene flow between pollock popu- lations. The genetic relationships are summarized from studies of differences in microsatellite allele distributions and from differences in mtDNA sequences. These studies indicate strong separation and little gene flow across the Pacific Ocean, and differences between the Gulf of Alaska and Bering Sea.
62 S.A. Macklin (ed.)

distances, standard genetic distance, and the Neighbor Joining Method will

be used. The DNA sequences from individuals will be aligned and compared

with software written to handle large numbers of sequences, and analyzed

using parsimony (PAUP), maximum likelihood (PHYLIP), and neighborjoining methods to construct phenograms as we have in our earlier analyses. Gene flow will be estimated using the phylogenetic approach of Slatkin

and Madison (1989). Population structure will be measured using the Gst

statistic (Takahata and Palumbi, 1985) which has been modified for DNA sequence analysis and tested against a random null model using bootstrapping

(Palumbi and Wilson, 1990). In the event that recombination within alleles

is detected, allele phylogenies will be constructed with genetic distance techniques (Slatkin and Madison, 1989). Coding regions will be examined for

patterns of amino acid versus silent nucleotide changes among individuals

(Hughes and Nei, 1988).

Although the mtDNA data was sufficient to differentiate between Asian

populations and American populations, it did not adequately detect more

finescale structure within these groups. As stated above, we therefore began

using DNA microsatellites to study this smaller scale population structure

of pollock.

Microsatellites are segments of DNA that consist of a small (2–5 bases)

motif repeated in tandem several times, such as GTGTGTGT. They have

been found to be useful for population studies in many organisms. Microsatellites often give a finer scale of resolution than other molecular genetic

markers.

Several microsatellite loci have already been found in pollock and other

related fishes. While we are still screening pollock populations for these loci

to determine which of them will be useful in this study, one microsatellite

locus, Gmo2, has been optimized for pollock, and yielded useful data. We

have studied 315 individual pollock from six localities at this locus. Our

results so far have identified 11 alleles ranging in length from 1 to 13 units.

Information derived from this one microsatellite locus revealed the same

detectable difference between Asian and American areas of the Bering Sea

that was detected by using the combined data from the sequences of the two

mitochondial loci, i.e., cytochrome-b, and ATPase-8. Moreover, this single

microsatellite locus also revealed a difference between the Gulf of Alaska

and Eastern Bering Sea populations that was not detectable using the two

mtDNA loci sequence data. Pairwise ANOVA comparisons (Table 2A.6)

suggest that the Aleutian Islands block some gene flow between the Pacific

and the Bering Sea. The consequence of this is that Gulf of Alaska fishes

appear to be mixing with western Pacific fishes nearly as much as with

Eastern Bering Sea fishes. A UPGMA dendrogram (Fig. 2A.3) shows the

relationship of the six localities according to genetic distance at the Gmo2

locus.

We have identified 13 more microsatellite loci that could provide the

discrimination between populations within each region that we have tried to

find for the past 3 years. We have already found that at least four of these

(pTCR-1, Gmo-1, Gmo-9, and Gmo-145) appear to be detectable in pollock

and highly variable.
Bering Sea FOCI Final Report 63

Table 2A.6: Pairwise ANOVA comparisons of Bering Sea and Gulf

of Alaska pollock populations based on polymorphism at the Gmo-2

microsatellite locus. Three distinct groups emerge: Eastern Bering

Sea, Western Bering Sea, and Gulf of Alaska.

Aleutian Shelikof

NE Shelf S. Kamchatka W. Bering Sea Basin Strait

NE Aleutians P=0.847 P=0.029 P=0.0002 P=0,700 P=0.0195

NE Shelf P=0.031 P=9.8E-5 P=0.831 P=0.030

S. Kamchatka P=0.308 P=0.025 P=0.056

W. Bering Sea P=0.0002 P=0.0001

Aleutian Basin P=0.036

If we can obtain additional funding, we would construct primers for PCR

(polymerase chain reaction) that are optimized to amplify these loci in pollock. Also, we would continue screening the other nine loci in order to

increase the number of usable markers for this study which could not only

provide finescale discrimination between pollock from each of the three geographical regions we have already identified, but these additional markers

would also allow us to calculate gene flow between populations.

References

Brooker, A.L., D. Cook, P. Bentzen, J.M. Wright, and R.W. Doyle (1994): Organization of microsatellites differs between mammals and cold-water teleost fishes.

Can. J. Fish. Aquat. Sci., 51, 1959–1966.

Hughes, A.L., and M. Nei (1988): Pattern of nucleotitle substitution at major

histocompatibility complex class I loci reveals over dominant selection. Nature,

335, 167–170.

Palumbi, S.R., and A.C. Wilson (1990): Mitochondrial DNA diversity in the sea

urchins Strongylocentrotus Purpuratus and S. Droebachiensis. Evolution, 44(2),

403–415.

Slatkin, M., and W.P. Maddison (1989): A cladistic measure of gene flow inferred

from the phylogenics of alleles. Genetics, 123, 603–613.

Takahata, N., and S.R. Palumbi (1985): Extranuclear differentiation and gene flow

in the finite island model. Genetics, 109, 441–457.
64 S.A. Macklin (ed.)
Bering Sea FOCI Final Report 65

Part 2B

Trends in north Pacific pollock and 1998 harvest

prognosis (Vidar G. Wespestad1)

Pollock

Walleye, or Alaska pollock, has been the basis of the largest groundfish

harvests since the early 1980s. The majority of the harvest is taken in

the U.S. and Russian EEZs, and relatively small amounts are harvested

off Canada, Japan, and Korea. However, in recent years there has been a

downward trend in harvest, primarily in the Russian EEZ. Pollock harvests

peaked in 1986 at 6.8 million t, declined until 1994, and in recent years

has been stable near 4 million t (Table 2B.1). One reason for the high

harvest levels in the 1980s was the advent of high seas fisheries in the Bering

Sea Donut Hole and in the Okhotsk Sea Peanut Hole (Fig. 2B.1). These

fisheries have been halted by international agreements, and are not expected

to resume operation in the near future.

North American catch has been stable, varying annually only slightly

from the 1981–1997 average of 1.3 million t. In Asia, on the other hand,

catch decreased significantly over the same time period, decreasing from a

peak of 5 million t in 1981 to 2.2 million t in 1994. Part of the decline

was due to overfishing, principally in Japan and Korea, and some in Russia,

including the Peanut Hole Fishery. A partial reason for the very low catches

observed in 1994 was the collapse of the Russian fishing industry, and their

inability to fully exploit pollock and other fish in the Russian EEZ. However,

harvesting capacity has increased in Russia and catch has been increasing in

recent years. In other areas of Asia, catches appear to remain at relatively

low levels, and where data are available, there do not appear to be any

prospects for near-term increases in stocks or harvest.

North American Pollock

The principal fisheries in North America are off Alaska, in the eastern Bering

Sea, and in the western Gulf of Alaska (Table 2B.1). Minor fisheries occur

in the eastern Gulf of Alaska and off Canada (Table 2B.1).

The eastern Bering Sea pollock fishery is the largest fishery in North

America, and has averaged a harvest of 1.2 million t since the early 1980s

(Fig. 2B.2, Table 2B.1). While catch has been stable, biomass has fluctuated

greatly in response to strong variation in recruitment. In the late 1970s and

early 1980s three strong year classes occurred which increased the population to very high levels in the mid-1980s (Fig. 2B.3). In the late 1980s to

early 1990s only one strong year-class occurred, 1989, and the population

declined to lower levels of abundance. This year, 1997, trawl surveys and

hydroacoustic-midwater trawl surveys of the eastern Bering Sea found that

the overall biomass of eastern Bering Sea pollock decreased slightly from

1Alaska Fisheries Science Center, NOAA, Seattle, WA 98115, U.S.A.
66 S.A. Macklin (ed.) Table 2B.1: Alaska pollock catch by area, 1981–1986, 1997 pre- liminary catch estimates, and 1998 preliminary catch recommen- dations. Russia: Russian Catch Only to 1993 Gulf of Eastern Donut Western Kamchatka North East South W. Sakhalin Peanut Korea Canada Alaska Bering Seaa Holeb Bering Sea East West Okhotsk Sakhalin Kuril I. Japan Sea Hole Japanc South North Total FAO 1981 5 148 1029 0 1133 329 482 102 82 260 67 0 665 166 1644 6112 4177 1982 5 169 1014 0 976 260 572 139 85 94 58 0 559 138 1365 5433 4478 1983 6 216 1040 0 1006 187 704 107 72 128 36 0 655 86 852 5095 4858 1984 6 307 1174 181 755 165 935 456 89 132 24 0 653 107 1058 6041 5986 1985 7 285 1198 363 662 121 975 540 82 97 27 0 632 85 838 5912 6132 1986 6 84 1189 1040 838 86 719 746 154 387 25 0 405 79 787 6545 6759 1987 7 62 888 1704 688 192 786 729 58 221 29 0 475 34 334 6206 6724 1988 6 56 1272 1484 1253 114 713 655 83 314 29 0 472 16 161 6628 6659 1989 6 73 1246 1484 961 123 791 687 47 316 53 0 477 24 0d 6287 6321 1990 5 78 1534 1069 573 186 537 946 40 375 42 0 454 27 0d 5866 5736 1991 5 83 1296 558 467 221 688 792 70 203 38 297 397 20 0d 5135 4893 1992 4 58 1218 10 596 253 760 509 14 161 43 698 358 15 0d 4698 4987 1993 4 106 1352 3 677 205 827 408 17 69 58 264 264 17 0d 4270 4617 1994 4 109 1422 0.6 382 104 733 608 25 17 36 124 258 11 0d 3833 4299 1995 4 77 1321 0.3 399 60 1074 915 1 5 29 NA NA 7 NA 3893 1996 4 53 1128 0.4 489 96 1250 756 49 19 18 Closed NA NA NA 3863 1997 4 74 1100 trace 757 55 1180 650 NA NA NA Closed 258 NA NA 4078 1998 98 1000 0.1 750 45 800 460 300 3453 Mean 120 1201 494 742 162 807 573 61 175 38 99 466 55 880 5288 5473 aIncludes Aleutian Islands bIncludes Bogoslof Island catch in U.S. EEZ cJapan catch: Fisheries Agency of Japan catch statistics: Local catch to 1986, 1987–1994 includes catch from Russian EEZ dPollock fishing prohibited since 1989 due to low stock abundance Gulf of Alaska and Bering Sea catches include discards in 1990–1996 Russian data from Fedeev, N.S. and V. Wespestad (in press), Harvest history of pollock (in Russian), and TINRO, Vladivostok, and KoTINRO, Petropavlovsk, Russia S. Korea catch: Jank Uk Lee, Natl. Fish. Res. Dev. Ag. (personal communication) N. Korea catch: C. Zhang Kunsan, Natl. U. (personal communication), estimated from ratio of north-south catch 1926–1940
Bering Sea FOCI Final Report 67

Figure 2B.1: Catch of pollock in Asia, North America, and the Donut Hole, 1981–1997.

1996, as expected, with a preliminary estimate of about 5.5 million t. However, the survey confirmed the presence of a very large 1996 year-class, which

was first noted by fishers during the 1997 pollock A season. The analysis is

not complete, but it appears that this year-class may be of similar size to

the 1978year-class which initiated the high abundance of the 1980s. The

1997 survey also found the 1985 year-class to be much bigger than previously

estimated. In 1996 Russian surveys reported 1995 to be a strong year-class

based on results from the northwest Bering Sea, but the same year-class was

not found to be abundant in U.S. waters. The large numbers of juvenile

fish suggest that the exploitable pollock stock will begin to increase in 1999–

2000. It should be noted that although eastern Bering Sea pollock are at a

relatively low level, the level of exploitation is currently less than 20%, much

below that of other major gadid stocks.

The western Gulf of Alaska is also increasing in abundance due to a

strong 1994 year-class. This year-class is entering the fishable population,

and the recommended allowable catch has been raised for 1998to 98,000 t,

up from 76,000 in 1997.

Aleutian Islands pollock, which appear to be a geographic extension of

eastern Bering Sea pollock, are stable or increasing. A 1997 survey indicates

that biomass has increased from a 1994 survey. The pollock size frequency

obtained in the survey indicates that the 1989 year-class is the dominant

age group. Aleutian Islands pollock quotas were halved in 1996 to 28,000 t.

Based on survey abundance estimates, the catch may remain at the current

level of 28,000 t. The Aleutian Islands pollock biomass may be an underestimate of actual abundance due to the lack of an estimate of the pelagic

portion of the population.

Adjacent to the Aleutian Islands is the Bogoslof Island area, which is the
68 S.A. Macklin (ed.)

Figure 2B.2: Pollock catch in the Gulf of Alaska and regions of the Bering Sea, 1981–1997.

primary spawning area of the Aleutian Basin/Donut Hole “stock.” These

pollock also continue to decline. In the 1997 survey the biomass was estimated to be near 300,000 t, down from 2.4 million t in 1988. Until the

“stock” increases to 1.1 million t no fishery will occur in the Bogoslof Island

area or in the Donut Hole. This level of biomass is not expected to occur

until 5–10 years from now, at the earliest, since it appears that Donut Hole

pollock mainly accrue from strong year-classes from the eastern and western

Bering Sea.

Asian Pollock

Pollock fisheries occur in the Japan Sea within the EEZs of Japan, Korea,

and Russia, on the Pacific side of Hokkaido. Stocks in these waters are

currently small, primarily due to overfishing. Recent official catch data is

scant (Table 2B.1). The greatest amount of catch is by Japan where the

catch quota was established as 258,000 t in 1997. South Korea has had very

small harvests in its EEZ in recent years, and the catch from North Korea is

unknown, although it is reported to have been closed since 1989 due to low

abundance. Russia also harvests relatively small amounts of pollock from

the Japan Sea and South Kurile Islands. The expected 1998harvest from

these and other minor stocks in Russian waters is estimated to be less than

300,000 t.

The primary harvest areas for pollock in Asia are in the Sea of Okhotsk

and northwestern Bering Sea. The Okhotsk Sea is the primary Asian harvest

area, and contains two main stocks, the northern Okhotsk, and west Kamchatka stocks. The preliminary estimate of the 1997 pollock catch in west

Kamchatka is 1.18million t, about equal to 1996. In the Northern Okhotsk
Bering Sea FOCI Final Report 69

Figure 2B.3: Eastern Bering Sea pollock abundance trend, 1964–1996.

the catch decreased slightly between 1996 and 1997, dropping to 650,000 t

from 756,000 t. For 1998, Russian biologists are recommending sharp reductions that would decrease the west Kamchatka catch to 800,000 t, and the

northern Okhotsk to 460,000 t. The 1998Russian pollock quotas are not

yet finalized, and it is possible that the final quotas may be different from

those recommended by scientists.

Scientists are concerned that the over-harvest in 1995–1996 reduced the

amount of mature pollock available in 1997, leading the fishery to harvest

small pollock. The problem of small fish also may have been caused by

regulations that prohibit trawling in the coastal spawning areas where adult

pollock congregate, forcing trawl vessels to fish immature pollock in offshore

areas.

The 1997 fishery was also reported to be affected by large area fishery

closures of areas with high bycatch of herring and undersized pollock. Adult

pollock abundance in Okhotsk Sea is expected to continue to decline in

1998. Russian data indicates that the 1995 year-class is a large year-class,

and 1992–1993 are near average. The oldest of these year-classes are just

reaching maturity, and the 1995 year-class will not mature until 2000.

The western-northern Bering Sea is the second largest producer in the

Russian EEZ. The catch of western Bering Sea stock used to average about

250,000 t, but in recent years has decreased to 50,000–70,000 t due to decrease in stock abundance and concentration of fishing effort in more productive areas such as the Okhotsk and northern Bering Sea. The recommended

catch quota for the western Bering Sea in 1998is up, increasing to 150,000 t.

The northern Bering Sea has the second largest quota in the Russian

EEZ, with a recommended 1998quota of 600,000 t. Pollock in this area

originate from the western Bering Sea and eastern Bering Sea stocks, and
70 S.A. Macklin (ed.)

Table 2B2: Estimated 1998harvest of walleye pollock by major

areas of the north Pacific.

Gulf of Bering Sea Kamchatka North South West

Alaska Eastern Western Northern West East Okhotsk Kurils Sakhalin Japan Korea Total

98 1000 150 600 800 45 460 300 3453

little to no spawning is observed in the area. Russian vessels have fished the

area since the early 1970s, and the catch has average near 500,000 t, with a

peak of 900,000 t in 1981.

This fishery is problematic for several factors, which include that the fish

are primarily of U.S. origin in recent years, the area (and the harvest) is

dominated by juvenile pollock that will recruit to U.S. fisheries at maturity,

there is little dialogue between the U.S. and Russia in developing a coherent

management plan, and there are questions on the level of Russian fisheries

monitoring in the area.

The magnitude of the harvest of small pollock in the Russian northern

Bering Sea is not fully known, but from reports of masters of vessels fishing

the area it may be significant. The effect on eastern Bering Sea stocks cannot

be fully determined at the present. Simulation of the catch and population

time series using likely scenarios of pollock movement suggests that the worst

case effect of the current levels of Russian fishing in the northern Bering Sea

is that harvest levels in the eastern Bering Sea may have to be reduced. This

will not lead to stock collapse in the eastern Bering Sea.

Russian scientists had been concerned that the percentage of undersized

pollock would increase in the 1998west Kamchatka fishery. However, they

believe new regulations may decrease the anticipated problems. In 1998,

for the first time, trawlers will be able to fish in selected coastal spawning

areas which will allow a harvest of large pollock. Secondarily, mesh size and

minimum retention size increases have been proposed which should further

reduce the harvest of juvenile fish. The mesh size and minimum retention

size increases also apply to the Bering Sea, so that catch of juvenile pollock

should also decrease in this area as well.

Prognosis Summary for 1998

The estimated projected harvest of pollock for 1998is shown in Table 2B.2.

The projected harvest is 3.4 million t. This is about 600,000 t less than

in 1997. A large part of the projected decrease is in the Sea of Okhotsk.

However, since quotas have not been finalized, it is not certain that these

reductions will occur. At last year’s Groundfish Forum, the 1997 pollock

harvest was forecast to be 3.8million t, slightly less than the actual harvest

of 4 million plus t. It is equally likely that this year’s pollock projection may

be on the conservative side.
Bering Sea FOCI Final Report 71

Part 3

Biophysical processes relevant to recruitment

dynamics of walleye pollock (Theragra chalcogramma)

in the Eastern Bering Sea (J.M. Napp,1 A.W.

Kendall, Jr.,1 and J.D. Schumacher2)

Abstract

Walleye pollock is a nodal species in the Bering Sea ecosystem (NRC Report

1996): juvenile pollock are the dominant prey of fishes, seabirds, and marine

mammals in this productive ecosystem. The estimated adult pollock biomass

in the eastern Bering Sea and central basin exceeds 9 MMT, and is the target

of an ∼$1 billion fishery.

We constructed a conceptual model for larval pollock dynamics using

factors we found to influence their distribution and feeding success in the

southeastern Bering Sea. These factors may have a strong influence on

recruitment success by modifying larval survival. The model is based on

relevant biophysical variables and pollock early life history traits. Pollock

spawning occurs in discrete concentrations during winter and spring in a

variety of habitats which include oceanic (basin and slope) and shelf waters.

Biophysical phenomena that affect conditions for larval survival and eventual recruitment exhibit marked differences between the Oceanic and Shelf

Regimes. In the Oceanic Regime 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 of these

eddies are transported onto the shelf, thereby providing larvae to the Outer

Shelf Domain. Observations from biophysical instrument platforms moored

over the basin demonstrated that advection rather than local production

dominated the observed springtime increase in chlorophyll (often a correlate

of larval food). Over most of the southeastern shelf eddies are absent and

other phenomena are important. Seasonal sea-ice and the associated cold

pool of bottom layer water are striking features of the Middle Shelf Domain.

Interannual variability in sea-ice and cold-pool 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.

3.1 Introduction

3.1.1 Description of the Area

The Bering Sea (Fig. 3.1) is a semi-enclosed portion of the North Pacific

Ocean that lies between the northernmost land masses of the North Amer1Alaska Fisheries Science Center, NOAA, Seattle, WA 98115, U.S.A.

2Pacific Marine Environmental Laboratory, NOAA, Seattle, WA 98115, U.S.A.
72 S.A. Macklin (ed.)

Figure 3.1: Southeast Bering Sea and associated biophysical domains. The solid circle indicate locations of

the BS FOCI biophysical platforms.
Bering Sea FOCI Final Report 73

ican and Asian continents. It is divided almost equally between a deep

basin (maximum depth 3,500 m) and a continental shelf (<200 m) which

are separated by a steep convoluted continental slope (Hood, 1981; Macklin,

in press). The Bering Sea is bounded to the south by the Aleutian Island

chain with its many passes and to the north by the shallow (<60 m) Bering

Strait, providing the only connection from the Pacific to the Arctic Ocean.

Water exchange between the North Pacific Ocean and the Bering Sea occurs mainly through the deeper western passes, although transport through

the eastern passes is important to regional circulation and water properties. The broad (>500 km) eastern shelf is the second broadest continental

shelf in the world. The southeastern Bering Sea consists of an Oceanic and

Shelf Regime (Fig. 3.1). Within the Shelf Regime, three distinct Domains

exist which are characterized by contrasts in water column structure, currents, and biota (Iverson et al., 1979a; Coachman, 1986; Schumacher and

Stabeno, in press). These Domains include the Coastal (<50 m deep with

weak stratification), Middle Shelf (50–100 m deep with strong stratification),

and Outer Shelf (100–200 m deep with mixed upper and lower layers separated by slowly increasing density). The zooplankton community in the

two shallower Domains is comprised primarily of the small copepods and

euphausiids whereas in the Outer Shelf Domain and in the Oceanic Regime

large open-ocean copepods are numerically dominant (Cooney and Coyle,

1982; Vidal and Smith, 1986).

Being a high-latitude sea, seasonal extremes occur in solar radiation

(length of daylight), meteorological forcing, and ice cover (Niebauer, 1981;

Overland, 1981). Interannual variations in ice extent (Mysak and Manak,

1989; Wyllie-Echeverria, 1995a) and its associated phenomenon, the cold

pool, are marked and interdecadal changes (sometimes called regime shifts

or Decadal Climate Oscillations: DCO) in the atmosphere above the North

Pacific Ocean affect the surface wind stress, Sverdrup transport, surface

ocean heat flux (Trenberth and Hurrell, 1995), and likely have significant

implications for the biota (Mantua et al., 1997).

3.1.2 Description of the Problem

The Bering Sea is the site of some of the most productive fisheries on Earth.

Besides the lucrative king crab, halibut, and salmon fisheries, most of the

world catch of walleye pollock comes from the Bering Sea. Pollock is the

most abundant species harvested in the Bering Sea, accounting for 80% of

the total weight of the harvest. Pollock, with a total biomass in the Bering

Sea approaching 20 MMT, is harvested in Bering Sea waters of the exclusive

economic zones (EEZ) of Russia and the U.S. Formerly there was a large

pollock fishery in international waters of the Bering Sea basin (known as the

“donut hole”), but it is now closed by international agreement. The annual

U.S. catch of pollock in the Bering Sea in recent years has amounted to

1.3 MMT, with an ex-vessel value of $210 million. Pollock also dominate the

ecosystem of the Bering Sea, providing most of the food for the extensive

marine mammal and bird populations found there (e.g., Springer and Byrd,

1989; Lowry et al., 1996; Sinclair et al., 1996).
74 S.A. Macklin (ed.)

Figure 3.2a: Distribution of selected walleye pollock life history stages in the southeastern Bering Sea. (a)

pollock spawning areas, 1984-1989 as defined by the fishery; fishing areas are the dark squares and the black

dots are where spawning fish were found (from Dell’Arciprete, personal communication).

Pollock in the Bering Sea do not form one homogeneous population, but

the actual stock structure is not well known. For example, distributions

of spawning adults, eggs, and larvae show a broad geographic range (Dell’

Arciprete, in preparation; Fig. 3.2). Research using spawning and juvenile

distributions and elemental composition of otoliths suggested that four populations were identifiable in the eastern Bering Sea (Mulligan et al., 1989).

More recent genetic studies, conducted as part of Bering Sea FOCI, indicate that there are differences between pollock from the eastern and western

parts of the Bering Sea (Bailey, this report). Within the eastern Bering

Sea, there are several spawning areas, and these may also be discrete stocks.

However, presently used genetic techniques are unable to detect significant

differences between spawning areas—genetic variability within subjectively

defined spawning areas is large relative to that between areas.

In the eastern Bering Sea there are large interannual variations in recruitment of pollock (more than one order of magnitude), and these drive

population size and thus harvest levels. Without reliable forecasts of recruit-
Bering Sea FOCI Final Report 75

Figure 3.2b: Distribution of selected walleye pollock life history stages in the southeastern Bering Sea. (b)

pollock eggs; fishing areas are the dark squares and the black dots are where spawning fish were found (from

Dell’Arciprete, personal communication).
76 S.A. Macklin (ed.)

Figure 3.2c: Distribution of selected walleye pollock life history stages in the southeastern Bering Sea. (c)

pollock larvae; fishing areas are the dark squares and the black dots are where spawning fish were found

(from Dell’Arciprete, personal communication).
Bering Sea FOCI Final Report 77

ment, based on an understanding of the processes that determine recruitment

variability, harvest levels must be set very conservatively. In order to understand recruitment variations, we must understand the relationships among

the various spawning populations, and the contribution of each to recruitment to the total stock. Recruitment in Bering Sea pollock, as in most other

marine fish, is thought to be largely set during their egg and larval stages.

Studies on causes of mortality of these early life history stages of pollock are

needed to understand recruitment variation.

3.2 Physical Oceanographic Setting

3.2.1 Marine Climatology and Sea Ice

Complex interactions among ocean, ice, and atmosphere dominate the physics

of the Bering Sea. The migration of storms results in a statistical feature

known as the Aleutian Low, one of the two main low pressure systems in

the high latitude northern hemisphere. During summer with its long periods

of daylight and high insolation, the Aleutian Low is typically weak and the

weather is benign. During the darkness of winter, a marked change occurs

in atmospheric pressure fields. The Asian continent is dominated by high

sea level pressure (Siberian High) while the Aleutian Low intensifies and

dominates weather over the North Pacific and Bering Sea. The juxtaposition of these features results in strong, frigid winds from the northeast.

The frequency and intensity of storms in the southern Bering Sea decreases

from winter to summer and frequency also decreases with increasing latitude (Overland and Pease, 1982). In the winter, an average of three to five

storms per month move eastward along the Aleutian Island Chain forming

the primary storm track, while less than two storms per month cross the

northern Bering Sea. A secondary storm track curves northward along the

Asian coast. A difference in the number of storms also occurs across the

broad eastern shelf, with more activity occurring over the Outer Shelf than

the Coastal Domain (Schumacher and Kinder, 1983).

Seasonal sea ice extent in the eastern Bering Sea fluctuates over 1000 km

between the Bering Strait in summer and south to the Alaska Peninsula and

shelf break in winter. The actual mechanism of ice formation for the eastern

shelf has been described by a “conveyor belt” analogy (Overland and Pease,

1982). Ice is produced along leeward (south-facing) coasts primarily located

in the northern region of the shelf, and driven by wind to its thermodynamic

limit where it melts. Brine rejection occurs as water freezes and regions of

open water, or polynyas, are created by downwind advection of ice. The sea

ice limit advances southward as ice-melt cools and freshens the upper ocean.

The amount of production and advection of ice depends upon which storm

track dominates in a given winter, with greatest ice production occurring in

years when the Aleutian Low is well developed and storms migrate along the

primary storm track.

Variations in overall ice coverage (Fig. 3.3), time of advection over the

open shelf, and subsequent melt-back are striking features of the physical

environment. Formation of sea ice generally begins in November, with max-
78 S.A. Macklin (ed.)

Figure 3.3: Time series of annual maximum sea ice extent, 1972 to 1997 (Wyllie-Echeverria and Wooster,

submitted). The index is the southernmost latitude of seasonal sea ice extent along longitude 169◦W in the

Bering Sea. The 26-year mean (57◦15

N) and standard deviation (±22) are shown as solid horizontal lines.

imum ice extent occurring in late March. Ice-free conditions typically exist from June through October. Observations of ice cover over the eastern

Bering Sea shelf show a nearly 40% interannual variation about the mean

(Niebauer, 1988). Other characteristics of ice cover that exhibit great variability include duration of ice at its southern extent (3–15 weeks), time of

retreat from the southernmost extent (between mid-March and June), and

number of weeks that ice remains over the Middle Shelf Domain (3–28weeks

with a mean of 20 weeks; Wyllie-Echeverria, 1995b).

Ice formation, brine rejection, advection, and eventual melting play a

critical role in fluxes of heat and salt and generation of both baroclinic flow

and the cold pool located over the Middle Shelf Domain (Schumacher and

Stabeno, in press; Wyllie-Echeverria, 1995b). The positive buoyancy from

melting ice initiates both baroclinic transport along the marginal ice zone

(∼0.3 × 106 m3 s−1) and stratification. Cooling and mixing associated with

ice advance help to condition the entire water column over the Middle Shelf

Domain and as seasonal heating occurs, the lower layer becomes insulated,

often with temperatures remaining below 2.0◦C (Reed, 1995). It is these

waters that are commonly called the “cold pool” and whose area varies by

∼20 × 104 km2 between maximum and minimum extent. Also associated

with ice-melt is a bloom of phytoplankton that accounts for 10–65% of the total annual primary production over the eastern shelf (Niebauer et al., 1990).
Bering Sea FOCI Final Report 79

Ice production and the cold pool also influence distributions of higher trophic

level biota (Ohtani and Azumaya, 1995; Wyllie-Echeverria, 1995a).

3.2.2 Oceanic Circulation

The major objectives for BS FOCI research on circulation over the basin

were to identify potential pathways which could connect the various pollock

stocks in the Bering Sea and to identify features and mechanisms which could

provide habitats that favor survival of larval fish and/or transport onto the

shelf. Prior to BS FOCI research many schematics existed of circulation in

the Bering Sea. In these, wind stress was considered to provide the primary

forcing (Hughes et al., 1974). Using observations (Stabeno and Reed, 1994;

Leben, personal communication; Stabeno et al., in press a) and model studies (Bond et al., 1994; Overland et al., 1994) conducted during BS FOCI, we

have greatly enhanced knowledge of currents and meteorological forcing. A

cyclonic gyre dominates circulation with a western boundary current (Kamchatka Current) along the Asian side of the basin (Fig. 3.4; Reed et al.,

1993; Cokelet et al., 1996) and the Bering Slope Current (BSC) forming the

eastern boundary (Stabeno and Reed, 1994; Stabeno et al., in press a). This

gyre is mainly an extension of the Alaskan Stream with the majority of volume transport (6–12 × 106 m3 s−1) entering through the eastern passes and

exiting via the Kamchatka Current (Stabeno and Reed, 1994). When instabilities in the Alaskan Stream inhibit flow into the Bering Sea through Near

Strait (Stabeno and Reed, 1992), transport in the Kamchatka Current can be

reduced by ∼50% and the alteration of flow can persist for months to years

(Reed and Stabeno, 1993). A climatology of the wind forcing shows that

eastward- and northward-propagating storm systems dominate the surface

stress at short periods (<1 month), which serves principally to mix the upper

ocean (Bond et al., 1994). At longer periods (>1 month), the wind-driven

transports estimated by the Sverdrup method account for roughly one-half

of the observed transport within the Kamchatka Current. The interannual

variations in the Sverdrup transports are ∼25% of the mean. Thus, while

wind driven transport contributes significantly to circulation, the Alaskan

Stream is the dominant circulation feature in the Bering Sea.

Results from BS FOCI studies described the previously unknown Aleutian North Slope Current (ANSC: Reed and Stabeno, in press) and a refined

view of the Bering Slope Current (BSC: Leben, personal communication;

Stabeno et al., in press a). Northward inflows of the Alaskan Stream through

Near Strait, Amchitka Pass, and Amukta Pass produce the ANSC, which is

an eastward flow along the north side of the Aleutian Islands. The ANSC is

often fairly narrow (<50 km) and shallow (upper 500 m) with peak speeds

>40 cm s−1. Eddy-like features occur in this region and some are formed

by flow through Amukta Pass (Schumacher and Stabeno, 1994). The ANSC

typically transports 2–4 × 106 m3 s−1, providing the main source of the BSC

and having a profound impact on regional water properties and circulation

(Schumacher and Stabeno, 1994; Reed and Stabeno, in press; Reed and

Stabeno, submitted). BS FOCI research also synthesized satellite altimetry, hydrographic, and satellite-tracked drifter data to elucidate features
80 S.A. Macklin (ed.)

Figure 3.4: Major current features and general circulation of the upper 50 m of the Southeast Bering Sea.

of the BSC. The BSC exists in two modes: an ill-defined, highly variable

flow interspersed with eddies, meanders, and instabilities, or a more regular

northwestward flowing current. It is likely that shelf/slope exchange differs

significantly depending upon which mode dominates in the BSC. The potential importance of both the ANSC and BSC to pollock larvae is twofold:

they can provide transport from the Oceanic Regime (including the important spawning region near Bogoslof Island) to the Outer Shelf Domain, and

their inherent eddies may provide a habitat that favors survival.

3.2.3 Eddies

Eddies are a ubiquitous feature of the southeastern Bering Sea (Schumacher

and Stabeno, 1994; Stabeno et al., in press a). During 3 years of BS FOCI

(1992, 1993, 1994) a moored instrument platform, named Peggy, was located in 2200 m of water over the southeastern Oceanic Regime (54◦48

N,

168◦34

W; Fig. 3.1). Data from this biophysical platform provided the most

complete time series of water properties and currents over the southeastern
Bering Sea FOCI Final Report 81

basin available to date. The results showed the marked influence of eddies on water properties, current velocity, and chlorophyll concentration and

permitted a characterization of the eddies as often being anti-cyclonic, 20–

100 km in diameter, and extending to a depth of 400–1000 m with rotational

speeds >20 cm s−1 (Fig. 3.5 and 3.6; Cokelet and Stabeno, 1997). Eddies

are also common at the eastern shelf break (Schumacher and Reed, 1992)

and shoreward to depths of ∼150 m. A recent interpretation of hydrographic

observations (Reed, submitted) suggests anticyclonic eddies exist in the region between 100 and 122 m <20% of the time. Shoaler than 100 m, eddies

are uncommon. Until recently, eddies were not considered to play a role in

Outer Shelf Domain dynamics. Between 1986 and 1994, 45 satellite-tracked

buoys were deployed in support of studies of pollock and their environment.

In three of these years, satellite-tracked buoys were deployed in areas where

larval pollock were abundant. In all four cases trajectories of the buoys defined eddies (Fig. 3.6). Conversely, the buoys (33) which were not deployed

in a larval patch did not indicate eddies. This association of pollock larvae

and eddies may have significant impact on larval survival (Schumacher and

Stabeno, 1994).

3.2.4 Exchange Between the Oceanic and Shelf Regimes

Shelf-slope exchange can occur virtually anywhere along >1200 km of shelf

break north of Unimak Pass; however, preferential transport onto the shelf

has been observed in two regions: Bering Canyon (along the Aleutian Islands near Unimak Pass) and west of the Pribilof Islands. The enhanced

concentration of nutrients observed near Unimak Pass likely originates from

ANSC waters interacting with canyon topography and coming onto the shelf

(Schumacher and Stabeno, in press). South of the Pribilof Islands the outer

shelf narrows and accelerates the flow along the 100 m isobath which then

turns northward (Stabeno et al., in press). This phenomenon likely results

in slope water being entrained onto the shelf from Pribilof Canyon (Schumacher and Stabeno, in press) and thereby provides a somewhat continuous

source of nutrients to the vicinity of the Pribilof Islands. Evidence for this

flow near the Pribilof Canyon is the on-shelf trajectories of satellite-tracked

drifters released over the canyon and the presence of Outer Shelf Domain

mesozooplankton taxa on the eastern side of the islands in the Middle Shelf

Domain (Stabeno et al., in press b; Napp et al., submitted).

Episodic events of onshelf flow have been observed resulting from both

eddy-topography interactions and instabilities in the BSC (VanMeurs and

Stabeno, in press). Along the slope of the central shelf (∼56.7◦N), current

records reveal that eddies are common and estimates of salt and temperature fluxes indicate that significant onshore fluxes exist (Schumacher and

Reed, 1992). In 1992 an excellent set of data was collected when an eddy

translated onto the shelf (Schumacher and Stabeno, 1994). Three satellitetracked drifters had been deployed in the center of an eddy. The drifters

remained in the eddy for weeks until the eddy translated onto the shelf. The

drifters were deposited onto the shelf as the eddy disintegrated. Both of

these episodic events of onshelf flow were related to the stability of the BSC
82 S.A. Macklin (ed.) Figure 3.5: Mesoscale eddies detected in the Bering Slope Current using moored instruments (Cokelet and Stabeno, 1997). Wind, density, and current at Peggy Bering Sea, spring 1992, showing the passage of eddies.
Bering Sea FOCI Final Report 83

Figure 3.6: A mesoscale eddy detected in the Bering Slope Current using Lagrangian drifters (Cokelet and

Stabeno, 1997). The satellite-tracked drifter was released in the vicinity of Peggy Bering Sea, spring 1992.
84 S.A. Macklin (ed.)

and are mechanisms that could transport both nutrients and pollock larvae

onto the shelf.

3.3 Production of Prey for Larval Pollock—Variability in

the Timing and Magnitude of the Spring Phytoplankton Bloom

Two of the Program’s hypotheses were (1) interannual variability in the

timing of prey production limits larval survival, and (2) prey densities in

the Oceanic Regime are generally less than those encountered in the Shelf

Regime. We assumed that production of most larval prey was initiated by the

spring phytoplankton bloom. Thus, the lower trophic level research component of BS FOCI had two main objectives: describe interannual variability

in the timing of spring phytoplankton blooms, and compare variability in

springtime standing stocks of larval pollock prey between the Oceanic and

Shelf Regimes. Variability in the timing and magnitude of the spring bloom

are reported in this section and variations in prey density are presented in

the larval feeding section.

Knowledge of spring phytoplankton bloom dynamics and the mesozooplankton community that produces prey for larval pollock is greatest for the

Shelf Regime (e.g., Iverson et al., 1979a; Dagg et al., 1984; Sambrotto et

al., 1986; Vidal and Smith, 1986). Knowledge of the phytoplankton dynamics and pollock prey densities in the Oceanic Regime are less well known,

although the mesozooplankton community, in general, is well known (e.g.,

Motoda and Minoda, 1974; Iverson et al., 1979b; Coyle et al., 1996). The

waters in the vicinity of the shelf break, between the two regimes, are thought

to be a region of sustained productivity during the spring and summer (a

“green belt”) due to continuous flux of nutrients into the euphotic zone

(Springer et al., 1996).

3.3.1 Oceanic Regime

Bering Sea FOCI’s major contribution to the study of plankton dynamics

and interannual variability in the Oceanic Regime resulted from the use

of moored biophysical platforms to obtain continuous time-series of phytoplankton biomass, measurements of associated physical forcing functions

(e.g., winds for mixing and incident radiation), and acoustically derived zooplankton biomass. Time-series of phytoplankton biomass were obtained using chlorophyll absorbance meters (ChlAM) attached at discrete depths in

the euphotic zone. During our long-term deployments contamination of the

signal due to instrument biofouling was minimized using new technology—

less hazardous chemical biocides and subtraction of absorbance in several

wavebands outside the peak absorbance of chlorophyll (Davis et al., 1997).

Seasonal changes in zooplankton biomass and vertical distribution were estimated from continuous records of 150 kHz ADCP backscatter (Cokelet et

al., in preparation).

In the spring of 1993 a slow and gradual increase in chlorophyll was interrupted by a sharp (four-fold), rapid (<1 day) increase (Fig. 3.7a; Cokelet
Bering Sea FOCI Final Report 85 Figure 3.7: Springtime (1993) Peggy Bering Sea observations of chlorophyll and zooplankton biomass showing a rapid change in conditions on 21 April indicating an advective event (Cokelet et al., in preparation). (a) Chlorophyll concentration (mg m−3) from two depths as a function of time; (b) ADCP-derived zooplankton biomass (mg DW m−3) as a function of depth and time.
86 S.A. Macklin (ed.)

et al., in preparation). A simultaneous increase in the mixed layer depth

and appearance of warmer surface water (3.75◦C) suggest that the large increase in phytoplankton biomass was due to advection rather than in situ

growth. Currents were weak (∼10 cm s−1) during this period, but rotated

from southwestward to eastward. Elevated concentrations at the mooring

persisted for ∼20 days before gradually returning to lower pre-event levels. The same pattern was observed in the spring of 1994, although the

rapid increase in chlorophyll was somewhat slower. Note that during the

1993 event, diel vertical migration of the zooplankton community radically

changed (Fig. 3.7b). Without net samples we are unable to say whether this

was due to a change in behavior by the pre-event assemblage or whether

a new assemblage of zooplankton with different behavior arrived with the

high chlorophyll waters. These Eulerian biological measurements support

the previous point that mesoscale physical variability over the continental

slope is important, and demonstrates that at times biological and physical

variability are strongly linked in this system. The Bering Slope Current is

eddy-rich and pollock larvae are sometimes found in association with these

eddies (Schumacher and Stabeno, 1994). To the extent that phytoplankton

biomass is a surrogate for increased production and standing stock of larval

prey, larvae that find themselves in these dynamic features may have a lower

probability of starvation than those outside such features.

3.3.2 Shelf Regime

BS FOCI’s major contributions to our knowledge of spring bloom dynamics

in the Shelf Regime resulted from our combined use of moored biophysical platforms and Lagrangian drifters equipped with optical sensors. The

platforms enabled us to observe previously unreported under-ice spring phytoplankton bloom dynamics. In 1995, when sea ice extent was much further

south than usual, we measured a single, large, early phytoplankton bloom

over the Middle Shelf Domain (∼72 m of water) that continued to develop

despite an unstable water column (Fig. 3.8; Stabeno et al., in press c). Note

the low water temperatures (–0.5◦C). Previous researchers have described

an initial ice-edge bloom stimulated by increased water column stability (ice

melt) followed by a main spring bloom that occurs when wind mixing from

storms erode the thin fresh surface layer and restore nutrients (e.g., McRoy

and Goering, 1974; Niebauer et al., 1990). In 1995, however, the bloom occurred despite an unstable water column and Lagrangian drifters equipped

with optical sensors did not detect a subsequent “main” bloom. Springtime

winds were not strong enough to erode the pycnocline that year and surface

nutrients were never replenished after the under-ice bloom.

In 1996, a year with minimal ice extent, the spring bloom was first detected by aircraft in the Outer, rather than Middle Shelf Domain as in the

previous year, but not until the first week of May (Cullen, personal communication). Thus, the presence or absence of sea ice and springtime winds

influence the timing, location, and number of spring blooms.
Bering Sea FOCI Final Report 87 Figure 3.8a: Dynamics of a spring phytoplankton bloom under sea ice on the southeastern Bering Sea shelf during an extremely heavy ice year, 1995 (Stabeno et al., in press). Both panels show temperature and currents as a function of depth and time (upper panel) and chlorophyll concentration (mg m−3) or fluorescence, salinity (PSU), and sea-ice presence as a function of time. (a) Middle Shelf Domain.
88 S.A. Macklin (ed.)

Figure 3.8b: Dynamics of a spring phytoplankton bloom under sea ice on the southeastern Bering Sea

shelf during an extremely heavy ice year, 1995 (Stabeno et al., in press). Both panels show temperature

and currents as a function of depth and time (upper panel) and chlorophyll concentration (mg m−3) or

fluorescence, salinity (PSU), and sea-ice presence as a function of time. (b) Outer Shelf Domain.
Bering Sea FOCI Final Report 89

3.4 Larval Pollock Feeding

Much of the information on walleye pollock larval feeding is based on studies

done in Shelikof Strait, Gulf of Alaska (Theilacker et al., 1996). There they

found that starvation can be a significant source of mortality (up to 32%

per day) for first-feeding larvae, up to about 6.5 mm in length. Larval

condition is closely related to the amount of food in the water; at prey

concentrations of less than 20 l−1, condition indices are low and mortality

elevated. Numbers of prey per gut is positively correlated with numbers

of prey in the water at prey densities of less than about 20 l−1 (Canino,

personal communication). First-feeding pollock larvae ingest particles of

maximum dimension 100–400 μm. Maximum prey size increases with the size

of fish, while the minimum prey size remains more or less constant (Nakatani,

1988). Our dietary studies are presently limited to prey items that leave

some sort of hard body part in the digestive tract. Pollock larvae ingest

items of known (e.g., copepod nauplii, rotifers) and unknown nutritional

value where inefficient or ineffectual digestion is suspected (e.g., copepod

eggs and phytoplankton). Laboratory studies have shown that pollock larvae

modify their swimming behavior in the presence of food: in prey they turn

more frequently, swim slower, and spend more time in a horizontal rather

than vertical orientation (Spring, 1996). Vertical movements in the absence

of food may facilitate locating concentrations of prey in a highly stratified

water column or in thin microlayers of food (Iverson et al., 1979b; Owen,

1981).

3.4.1 Oceanic Regime

As in other areas, copepod nauplii were the most common food item in the

guts of first-feeding pollock larvae in the Oceanic Regime (bottom depth

1900 m) in April 1992 (Hillgruber et al., 1995). A suite of ca. 5 genera

of copepod nauplii (Eucalanus, Metridia, Pseudocalanus, Microcalanus, and

Oithona) were available in the water, 1992–1995. Concentrations ranged

from <5 to >40 liter−1 (Paul et al., 1996; Napp et al., in preparation).

Cyclopoid nauplii (Oithona spp.) tended to dominate the assemblage in all

years and most depths. Larval pollock, however, preferred the later stages

(NIII–NV) of calanoid nauplii over the more abundant cyclopoid nauplii and

earlier stages of calanoid nauplii (Hillgruber et al., 1995). In particular, they

selected for the older stages of the genera Metridia and Microcalanus, but

against Oithona. Late stage Oithona and Microcalanus nauplii are approximately the same size; therefore, this demonstrates prey selection on a basis

other than size. Copepod eggs were also prevalent in the guts, but they are

probably of little nutritional value, may have inordinately long gut residence

times, and may indicate a generally poor feeding environment (Flinkman et

al., 1994).

In 1992, larvae and their prey were most abundant at 30 m, where light

was sufficient for feeding (Fig. 3.9). At that depth, 97.5% of the larvae

were feeding, and they contained an average of 4.6 prey per larva. Densities

of copepod nauplii were 26.3 l−1 at 30 m; however, >80% of the available
90 S.A. Macklin (ed.)

Figure 3.9: Vertical distributions of larval pollock, larval length, prey concentration, feeding incidence, and

prey per larval gut for larvae collected in the Oceanic Regime, April 1992 (Hillgruber et al., 1995).
Bering Sea FOCI Final Report 91

nauplii were Oithona spp. (Hillgruber et al., 1995). Naupliar densities and

feeding incidence were much lower at other depths, leading to the conclusion

that overall, prey were below saturation densities at that station. This, along

with modeling results (Bollens et al., in preparation) leads us to explore the

possibility that protozoans could be an additional source of nutrition for

pollock larvae. Microzooplankton abundance (protozoans >20 μm) in the

Oceanic Regime in April 1992 ranged from 300–6233 organisms l−1 (0.58–

9.7 μgCl−1; Howell-K ̈ubler et al., 1996). Thus, in some situations, first

feeding pollock larvae could potentially meet their maintenance ration by

grazing on both protozoa and nauplii. Whether or not significant ingestion

of protozoa occurs in the field is not yet known, but a new technique for live

staining protists was developed and used to show that pollock larvae ingest

protozoa in the laboratory (Lessard et al., 1996; cf. Last, 1978).

3.4.2 Shelf Regime

The feeding environment of larval pollock in the Shelf Regime was investigated using samples collected at 2-week intervals in an area of high concentration of pollock larvae in late April and mid and late May 1995 (Brase, 1996).

The highest densities of pollock larvae were found in mid May (Fig. 3.10).

Mean standard lengths of larvae were 6.13 mm in late April, 6.40 mm in mid

May, and 7.37 mm in late May. The temperatures at the depths of maximal

larval abundance were 2.5◦C in late April, 3.5◦C in early May, and 3.75◦C

in late May (Fig. 3.10). Total copepod naupliar densities were always less

than 8l−1; maximum water column integrated abundance was in late May.

In most samples, 100% of the larvae were feeding. Copepod eggs were usually the most numerous prey item, with Pseudocalanus spp. nauplii being

the second most abundant item (Fig. 3.11). In late April 41% of the diet

by numbers, excluding copepod eggs, was rotifers, in mid May euphausiid

nauplii made up a significant fraction of the diet (24% by number, 64% by

volume), and in late May copepod nauplii (Pseudocalanus spp. and Acartia

spp.) were abundant in the larval diets (25% by number, 35% by volume).

First-feeding larvae (5.0–6.9 mm), however, had very few prey items in their

guts when copepod eggs were excluded from the analysis (April, 1 larva−1;

mid May 0.5–1 larva−1; late May, 3–5 larva−1).

In conclusion, it seems that in 1995 there was a mismatch between the

period of maximal first feeding larval abundance (the period of greatest

vulnerability to starvation) and the maximum standing stock of copepod

nauplii. During the period of maximal abundance of first feeding larvae

prey densities were much less than 20 l−1, the critical value determined from

research in Shelikof Strait. Evidence for a deleterious effect of low prey

concentrations on larvae was contrary to expectations. We lack specific estimates of larval mortality; however only 1% of the larvae sampled during mid

May 1995 were starving (Porter and Theilacker, in preparation). In Shelikof

Strait, at comparable prey densities (but slightly higher water temperatures)

ca. 34% of the first feeding larvae were starving. A late larval/early juvenile

survey of the Shelf Regime during the summer of 1995 revealed much lower
92 S.A. Macklin (ed.) Figure 3.10: Springtime vertical distributions of larval pollock (horizontal bars), copepod nauplii (filled circles), and water temperature (solid line; ◦C) at three stations over the southeastern shelf during a year of maximal ice extent (1995). Shown are the mean concentrations ± SE (pollock; Brase, 1996) and ±95% confidence interval (nauplii; Napp et al., in preparation). Station 1, late April; Station 2, early May; Station 3, late May.
Bering Sea FOCI Final Report 93 Figure 3.11: Larval gut contents by station and larval length during late April (Station 1) and early and late May (Stations 2 and 3, respectively), 1995 (Brase, 1996).
94 S.A. Macklin (ed.)

late larval/age-0 juvenile abundances than found in 1996, a minimal ice year

(Brodeur, this volume).

3.5 Implications: Shelf and Oceanic Regimes as Feeding Environments for Pollock Larvae

Now that we know what pollock larvae eat and which prey they prefer, we

can compare the two Regimes (Shelf and Oceanic) and examine interannual

differences in the timing of the spring phytoplankton bloom and prey standing stocks. Note that our investigations of prey density and spring bloom

dynamics were geographically and temporally limited. Prey density and larval feeding measurements were limited to places and times where pollock

larvae were very abundant and feeding studies were conducted. Spring phytoplankton bloom dynamics data were limited to the locations of the biophysical platforms which were initially chosen to be representative of particular

regions. In addition, our ability to resolve sources of interannual variability

is tempered by the short duration of the Program and the emphasis on two

large oceanographic regimes. We spent only two full field seasons in each

region with a transition year between. Thus our intra-Regime interannual

comparisons are limited to two adjacent years.

3.5.1 Timing of Prey Production

Egg production of many calanoid copepods is generally thought to be initiated by increased food availability (i.e., coincident with the spring phytoplankton bloom; e.g., Hirche, 1996). Our time-series observations of chlorophyll concentration (1993–1996) at the biophysical platforms suggest that

the onset of larval prey production was less variable over the basin than over

the shelf, despite the importance of mesoscale variability over the slope.

The presence or absence of sea-ice was the physical factor most responsible

for variability in timing over the shelf; variability in wind mixing may be

important, but only when ice is absent (cf. Sambrotto et al., 1986).

The assumption that production of prey is initiated by the spring bloom

remains to be tested for the Bering Sea. Recent examination of one species

of shelf prey producer (Calanus marshallae) revealed no correspondence between gonadal maturity (a proxy for egg production) and sea surface chlorophyll in April of 1995 (Baier and Napp, in preparation). In this species,

most of the sampled population was sexually mature females with well developed eggs in their oviducts ready for release, despite very low sea surface

chlorophyll values (0.5–1 μg l−1).

The timing of egg production relative to the appearance of first-feeding

larvae is also important. At 3◦C, a typical springtime temperature for the

Outer Shelf and Slope Domains, Metridia pacifica needs ca. 12 days to develop from egg to the fourth naupliar stage (NIV; Pinchuk and Paul, 1998)

and Pseudocalanus spp. require ca. 15 days to do the same (Corkett and

McLaren, 1978). The “critical period” of first feeding larvae is ca. 7–14 days

at 5◦C; therefore prey production must be initiated several weeks before first

feeding larvae appear.
Bering Sea FOCI Final Report 95

3.5.2 Amount of Prey Produced

Production of preferred prey involves two steps: egg production and development to the preferred developmental stage. Both are affected by variability in the physical environment. Total production of prey items may be

decoupled from the absolute level of primary production depending on the

amount of food required for maximal reproduction by the dominant calanoid

copepods in the system (Runge, 1988). Egg production rates by one of the

copepod genera responsible for prey production (Pseudocalanus spp.) would

not be food-limited in either region (slope or shelf) during periods of maximal phytoplankton standing stock. This may not be true for the larger

prey-producing copepods Metridia, Calanus, and Eucalanus.

Variability in prey densities within the Oceanic Regime and between

the Oceanic and Shelf Regimes was found to be much larger than initially

thought. We did find low densities over the Oceanic Regime of <10 nauplii l−1 in April of all years (Paul et al., 1996; Napp et al., in preparation),

but also found several incidences where densities were >20 l−1, the critical

value determined for larvae from Shelikof Strait. Naupliar abundances over

the shelf in April 1994 and 1995 and May 1995 were ≤10 l−1 at almost all

sampled depths. Our Oceanic Regime prey densities are comparable to the

slope values from PROBES with the exception of low values found in their

cold year, 1980 (Dagg et al., 1984; Walsh and McRoy, 1986). Shelf Regime

naupliar densities sampled during cold years are comparable between the

two programs, but BS FOCI did not sample the Shelf Regime in May and

June of “warm” years. One important distinction between the results of the

two programs is that BS FOCI has direct measurements of larval condition.

Even at low prey densities found during cold years by both programs, larvae

did not appear to be starving (Porter and Theilacker, in preparation).

Determination of prey density during the critical first feeding period is

only one part of the recruitment story. Exposure to high prey concentrations

is advantageous for rapid growth and potentially lower predation risk during

the larval and early juvenile stages. Over the Middle Shelf Domain, in the

absence of wind mixing, a rapid increase, then decline of phytoplankton and

nutrients is observed. Springtime water column stratification separates the

phytoplankton from their nutrient source. When nutrients become depleted

the bloom sinks and continued prey production by copepods must rely on

lower levels of phytoplankton standing stock sustained by regenerated nutrients. Thus, variability in insolation (heat flux) and wind mixing determines

the absolute or annual level of larval prey production over parts of the shelf.

3.5.3 Taxonomic Composition of Prey

Since we know that pollock larvae are selective feeders, we must take into

account the type of prey as well as the concentration of all available prey. A

major difference between the Oceanic Regime and Shelf Regime is the ratio

of calanoid to cyclopoid nauplii. At most depths sampled over the Oceanic

Regime in April of 1994, 20–30% of the copepod nauplii were calanoids, while

at the Outer Shelf Domain station on the same cruise, 50–60% were calanoid
96 S.A. Macklin (ed.)

nauplii. The exception to this generalization for the slope region was at the

depths where large concentrations of nauplii were found; they were 70%

calanoid, i.e., more similar to the Shelf Regime, than the Oceanic Regime

prey assemblage. Thus, when we take preferential feeding into account,

starvation was not apparent even at very low effective prey concentrations.

3.5.4 Larval Condition

In the above discussion we noted that we have little or no evidence to support

the hypothesis that starvation was an important source of mortality for

larval pollock in the Bering Sea (one might argue that these data refute the

hypothesis). Our limited measurements of larval condition were made in

patches of water where larvae were abundant. Few larvae showed symptoms

of recent food deprivation in these patches. However, these same larvae

were feeding under prey-poor conditions and had few prey items in their

guts. This contradiction, low prey levels, yet low incidence of starvation, is

one of the more significant findings of BS FOCI. Investigations are underway

to determine the affect of temperature on both prey production and larval

feeding and metabolism.

3.6 Conclusions

Pollock spawn in two distinct Regimes in the Southeast Bering Sea: the

Oceanic Regime and the Shelf Regime. At present, molecular genetic techniques are unable to distinguish between spawning fish in either regime or

among the fish regularly found spawning at different times and locations on

the southeastern shelf. Conditions for the emerging larvae can be very different for the two regimes as are the factors that affect variability in survival of

early larvae between regimes (Fig. 3.12). In the Oceanic Regime advection

is strong, but variable, and mesoscale features (eddies) are common. Conditions outside mesoscale features show very low interannual variability. Over

the shelf advection is generally low, but there are large fluctuations in the

environment due to interannual variability in the presence or absence of sea

ice. This affects the stability and temperature of the water column. Spring

phytoplankton bloom dynamics vary between the two regimes as a result

of the differences in their physical characteristics. Variability in observed

plankton standing stocks may be largely due to advective rather than local

processes in the Oceanic Regime. In the Shelf Regime interannual variability

in a complex set of forcing functions (sea ice, wind mixing, temperature, and

insolation) result in phytoplankton blooms with different timing, magnitude,

and transfer efficiencies to the zooplankton and nekton (or benthos). The

two Regimes provide different feeding environments for larval pollock. In the

Oceanic Regime prey concentrations are generally low and are dominated by

less preferable prey items. This may necessitate the larvae supplementing

their diet with protists. Mesoscale features of unknown origin, when present,

may contain much higher prey densities with a larger proportion of the prey

being the type preferred by first-feeding larvae. In the Shelf Regime, preferred prey constituted a larger fraction of the available prey, but copepod
Bering Sea FOCI Final Report 97 Figure 3.12: Switch model of walleye pollock early larval dynamics in the southeastern Bering Sea. Each box represents a life history stage through which survivors must pass. Biophysical processes thought to be important regulators of survival variability as a result of BS FOCI research are shown separately for the Oceanic and Shelf Regimes.
98 S.A. Macklin (ed.)

nauplii were still at minimal levels for growth and survival. There was no

evidence to suggest, however, that these larvae were starving. Low temperatures associated with early sea-ice-associated spring phytoplankton blooms

resulted in a mismatch between the maximal concentrations of first feeding

larvae and their prey (cf. Walsh and McRoy, 1986; Townsend et al., 1994).

Thus the key to interannual variation in food for first feeding pollock larvae

in the Oceanic Regime is advection, and in the Shelf Regime it is the coupled

dynamics of the atmosphere-ice-ocean system.

3.7 Acknowledgments

We thank the Principal Investigators of BS FOCI for allowing us use of their published and unpublished results, and the FOCI Coordinator, S.A. Macklin, for facilitating the Program’s research. We also express our thanks to the officers and crew

of the NOAA Ships Miller Freeman and Surveyor for their field support during the

Program.

3.8 References

Aron, W., and J. Balsiger (1989): Proceedings of the International Scientific Symposium on Bering Sea Fisheries. NOAA Tech. Memo. NMFS-F/NWC-163, 424

pp.

Baier, C.T., and J.M. Napp. Springtime distribution and gonadal maturity of

Calanus marshallae over the southeastern Bering Sea shelf (in preparation).

Bollens, S.M., M.C. Landsteiner, B.W. Frost, K.M. Bailey, and C.S. Davis. A model

of the upper ocean production dynamics of zooplankton and larval pollock in

the Bering Sea (in preparation).

Bond, N.A., J.E. Overland, and P. Turet (1994): Spatial and temporal characteristics of the wind forcing of the Bering Sea. J. Clim., 7, 1119–1130.

Brase, A.L.J. (1996): Temporal variation in feeding of larval walleye pollock, Theragra chalcogramma, in the southeastern Bering Sea. Master of Science Thesis,

University of Alaska, Fairbanks, 87 pp.

Coachman, L.K. (1986): Circulation, water masses, and fluxes on the southeastern

Bering Sea shelf. Cont. Shelf. Res., 5, 23–108.

Cokelet, E.D., R.F. Davis, and J.M. Napp. Springtime biophysical observations over

the southeastern Bering Sea continental slope: advection versus local changes

in chlorophyll and derived zooplankton biomass (in preparation).

Cokelet, E.D., J.M. Napp, and D. Dougherty. ADCP backscatter calibration for

Bering Sea zooplankton (in preparation).

Cokelet, E.D., M.L. Schall, and D. Dougherty (1996): ADCP-referenced geostrophic

circulation in the Bering Sea basin. J. Phys. Oceanogr., 26, 1113–1128.

Cokelet, E.D., and P.J. Stabeno (1997): Mooring observations of the thermal structure, density stratification and currents in the SE Bering Sea basin. J. Geophys.

Res., 102(C10), 22,947–22,967.

Cooney, R.T., and K.O. Coyle (1982): Trophic implications of cross-shelf copepod

distributions in the southeastern Bering Sea. Mar. Biol., 70, 187–196.

Corkett, C.J., and I.A. McLaren (1978): The biology of Pseudocalanus. Adv. Mar.

Biol., 15, 1–231.

Coyle, K.O., V.G. Chavtur, and A.I. Pinchuk (1996): Zooplankton in the Bering

Sea: A Review of Russian-Language Literature. In Ecology of the Bering Sea—

A Review of the Russian Literature, O.A. Mathisen and K.O. Coyle (eds.),

Alaska Sea Grant Report No. 96-01, Fairbanks, AK, 97–133.
Bering Sea FOCI Final Report 99

Dagg, M.J., M.E. Clarke, T. Nishiyama, and S.L. Smith (1984): Production and

standing stock of copepod nauplii, food items for larvae of the walleye pollock

Theragra chalcogramma in the southeastern Bering Sea. Mar. Ecol. Prog. Ser.,

19, 7–16.

Davis, R.R., C.C. Moore, J.R.V. Zaneveld, and J.M. Napp (1997): Reducing the

effects of fouling on chlorophyll estimates derived from long-term deployments

of optical instruments. J. Geophys. Res., 102(C3), 5851–5856.

Flinkman, J., I. Vuorinen, and M. Christiansen (1994): Calanoid copepod eggs

survive passage through fish digestive tracts. ICES J. Mar. Sci., 51, 127–129.

Hillgruber, N., L.J. Haldorson, and A.J. Paul (1995): Feeding selectivity of larval

walleye pollock Theragra chalcogramma in the oceanic domain of the Bering

Sea. Mar. Ecol. Prog. Ser., 120, 1–10.

Hirche, H.-J. (1996): The reproductive biology of the marine copepod, Calanus

finmarchicus—A review. Ophelia, 44, 111–128.

Hood, D.W. (1981): Introduction. In The Eastern Bering Sea Shelf: Oceanography and Resources, D.W. Hood and J.A. Calder (eds.), Vol. 1, University of

Washington Press, Seattle, xiii–xviii.

Howell-Kubler, A.N., E.J. Lessard, and J.M. Napp (1996): Springtime protozoan

abundance and biomass in the southeastern Bering Sea and Shelikof Strait,

Alaska: Its potential role as prey for planktivorous fish larvae. J. Plankton

Res., 18, 731–745.

Hughes, F.W., L.K. Coachman, and K. Aagaard (1974): Circulation, transport and

water exchange in the western Bering Sea. In Oceanography of the Bering Sea,

D.W. Hood, and E.J. Kelley (eds.), Occasional Publ. No. 2, Institute of Marine

Science, University of Alaska, Fairbanks, 3–37.

Iverson, R.L., L.K. Coachman, R.T. Cooney, T.S. English, J.J. Goering, G.L. Hunt,

Jr., M.C. McCauley, C.P. McRoy, W.S. Reeburg, and T.E. Whitledge (1979a):

Ecological significance of fronts in the southeastern Bering Sea. In Ecological

Processes in Coastal and Marine Systems, R.J. Livingston (ed.), Plenum Press,

New York, 437–466.

Iverson, R.L., T.E. Whitledge, and J.J. Goering (1979b): Chlorophyll and nitrate

fine structure in the southeastern Bering Sea shelf break front. Nature, 281,

664–666.

Last, J.M. (1978): The food of three species of gadoid larvae in the Eastern English

Channel and Southern North Sea. Mar. Biol., 48, 377–386.

Lessard, E.J., M.P. Martin, and D.J.S. Montagnes (1996): A new method for livestaining protists with DAPI and its application as a tracer of ingestion by

walleye pollock (Theragra chalcogramma (Pallas)) larvae. J. Exp. Mar. Biol.

Ecol., 204, 43–57.

Lowry, L.F., V.N. Burkanov, and K.J. Frost (1996): Importance of walleye pollock, Theragra chalcogramma, in the diet of phocid seals in the Bering Sea and

northwestern Pacific Ocean. In Ecology of Juvenile Walleye Pollock, Theragra chalcogramma, R.D. Brodeur, P.A. Livingston, T.R. Loughlin, and A.B.

Hollowed (eds.), NOAA Tech. Report NMFS 126, 141–152.

Macklin, S.A. Bering Sea FOCI. In The Bering Sea: A Summary of Physical, Chemical and Biological Characteristics and a Synopsis of Research, T.R. Loughlin and

K. Ohtani (eds.), North Pacific Marine Science Organization, PICES, Alaska

Sea Grant Press (in press).

Mantua, N.J., S.R. Hare, Y. Zhang, J.M. Wallace, and R.C. Francis (1997): A Pacific interdecadal climate oscillation with impacts on salmon production. Bull.

Amer. Met. Soc., 78, 1069–1079.

McRoy, C.P., and J.J. Goering (1974): The influence of ice on the primary productivity of the Bering Sea. In Oceanography of the Bering Sea with Emphasis on
100 S.A. Macklin (ed.)

Renewable Resources, D.W. Hood, and E.J. Kelley (eds.), Occasional Publ. No.

2, Institute of Marine Science, University of Alaska, Fairbanks, 403–421.

Motoda, S., and T. Minoda (1974): Plankton of the Bering Sea. In Oceanography

of the Bering Sea with Emphasis on Renewable Resources, D.W. Hood, and E.J.

Kelley (eds.), Occasional Publ. No. 2, Institute of Marine Science, University of

Alaska, Fairbanks, 207–241.

Mulligan, T.J., K. Bailey, and S. Hinckley (1989): The occurrence of larval and

juvenile walleye pollock, Theragra chalcogramma, in the eastern Bering Sea with

implication to stock structure. In Proceedings of the International Symposium

on the Biological Management of Walleye Pollock, Alaska Sea Grant Report

No. 89-1, 471–489.

Mysak, L.A., and D.K. Manak (1989): Arctic sea-ice extent and anomalies, 1953–

1984. Atmos. Ocean, 27, 376–405.

Nakatani, T. (1988): Studies on the early life history of walleye pollock, Theragra

chalcogramma, in Funka Bay and vicinity, Hokkaido. Mem. Fac. Fish. Hokkaido

Univ., 35, 1–46.

Napp, J.M, R.D. Brodeur, D. Demer, R. Hewitt, P.J Stabeno, G.L Hunt, Jr., and

J.D. Schumacher. Determination of nekton, zooplankton and seabird concentrations at tidally generated shelf fronts in the eastern Bering Sea. Mar. Ecol.

Prog. Ser. (submitted).

Napp, J.M., A.J. Paul, L.J. Haldorson, and M.K. Cohen. Interannual variability

of larval pollock feeding and prey in the southeastern Bering Sea, I, Copepod

naupliar distributions and effective prey concentrations (in preparation).

National Research Council Committee on the Bering Sea Ecosystem (1996): The

Bering Sea Ecosystem. National Academy Press, Washington, D.C., 324 pp.

Niebauer, H.J. (1981): Recent short-period wintertime climatic variations and their

effect on sea-surface temperatures in the eastern Bering Sea. In The Eastern

Bering Sea Shelf: Oceanography and Resources, D.W. Hood, and J.A. Calder

(eds.), Vol. 1, University of Washington Press, Seattle, WA, 23–30.

Niebauer, H.J. (1988): Effects of El Ni ̃no-Southern Oscillation and North Pacific

weather patterns on interannual variability in the subarctic Bering Sea. J.

Geophys. Res., 93, 5051–5068.

Niebauer, H.J., V.A. Alexander, and S. Henrichs (1990): Physical and biological

oceanographic interaction in the spring bloom at the Bering Sea marginal ice

edge zone. J. Geophys. Res., 95, 22,229–22,242.

Ohtani, K., and T. Azumaya (1995): Interannual change of the sea conditions on

the continental shelf and its influence on abundance of walleye pollock in the

eastern Bering Sea. Can. J. Fish Aquat. Sci., Special Pub. 121, 87–95.

Overland, J.E. (1981): Marine climatology of the Bering Sea. In The Eastern

Bering Sea Shelf: Oceanography and Resources, D.W. Hood, and J.A. Calder

(eds.), Vol. 1, University of Washington Press, Seattle, 15–22.

Overland, J.E., and C.H. Pease (1982): Cyclone climatology of the Bering Sea and

its relation to sea ice extent. Mon. Weather Rev., 110, 5–13.

Overland, J.E., M.C. Spillane, H.E. Hurlburt, and A.J. Wallcraft (1994): A numerical study of the circulation of the Bering Sea basin and exchange with the

North Pacific Ocean. Phys. Oceanogr., 24, 736–758.

Owen, R.W. (1981): Microscale plankton patchiness in the larval anchovy environment. Rapp. P.-v. Reun. Cons. Int. Explor. Mer., 178, 364–368.

Paul, A.J., J.M. Paul, and K.O. Coyle (1996): Abundance and taxa composition of

copepod nauplii over southeastern Bering Sea deep water spawning grounds of

walleye pollock, Theragra chalcogramma. Crustaceana, 69, 494–508.

Pinchuk, A.I., and A.J. Paul (1998): Growth of Metridia pacifica (Copepoda:

calanoida) nauplii in the laboratory. Plankton Biol. Ecol., 45(2) (in press).
Bering Sea FOCI Final Report 101

Porter, S.M., and G.H. Theilacker. Physiological condition of walleye pollock larvae, Theragra chalcogramma, in the southeastern Bering Sea using histological

techniques (in preparation).

Reed, R.K. (1995): Water properties over the Bering Sea shelf: climatology and

variations. NOAA Tech. Rept. ERL 452-PMEL 42, 15 pp.

Reed, R.K. Confirmation of a convoluted flow over the southeastern Bering Sea

Shelf. Cont. Shelf Res. (in press).

Reed, R.K., G.V. Khen, P.J. Stabeno, and A.V. Verkhunov (1993): Water properties

and flow over the deep Bering Sea basin, summer 1991. Deep-Sea Res., 40,

2325–2334.

Reed, R.K., and P.J. Stabeno (1993): The return of the Alaskan Stream to Near

Strait. J. Mar. Res., 51, 515–527.

Reed, R.K., and P.J. Stabeno (1996): On the climatological mean circulation over

the eastern Bering Sea shelf. Cont. Shelf Res., 16, 1297–1305.

Reed, R.K., and P.J. Stabeno. The Aleutian North Slope Flow. In The Bering Sea:

A Summary of Physical, Chemical and Biological Characteristics and a Synopsis

of Research, T.R. Loughlin, and K. Ohtani (eds.), North Pacific Marine Science

Organization, PICES, Alaska Sea Grant Press (in press).

Reed, R.K., and P.J. Stabeno. Magnitude and time scales of inflow through Unimak

Pass, Alaska. Geophys. Res. Lett. (submitted).

Runge, J.A. (1988): Should we expect a relationship between primary production

and fisheries? The role of copepod dynamics as a filter of trophic variability.

Hydrobiolgia, 167/168, 61–71.

Sambrotto, R.N., H.J. Niebauer, J.J. Goering, and R.L. Iverson (1986): Relationship among vertical mixing, nitrate uptake, and phytoplankton growth during

the spring bloom in the southeast Bering Sea middle shelf. Cont. Shelf Res., 5,

161–198.

Schumacher, J.D., and A.W. Kendall, Jr. (1995): An example of fisheries oceanography: walleye pollock in Alaskan waters. Rev. Geophys. Suppl., 33, 1153–1163.

Schumacher, J.D., and T.H. Kinder (1983): Low-frequency current regimes over the

Bering Sea shelf. J. Phys. Oceanogr., 13, 607–623.

Schumacher, J.D., and R.K. Reed (1992): Characteristics of currents over the continental slope of the eastern Bering Sea. J. Geophys. Res., 97, 9423–9433.

Schumacher, J.D., and P.J. Stabeno. The continental shelf of the Bering Sea. In

The Sea, Vol. XI, The Global Coastal Ocean: Regional Studies and Synthesis.

John Wiley, Inc., New York (in press).

Schumacher, J.D., and P.J. Stabeno (1994): Ubiquitous eddies of the eastern Bering

Sea and their coincidence with concentrations of larval pollock. Fish. Oceanogr.,

3, 182–190.

Sinclair, E.H., G.A. Antonelis, B.W. Robson, R.R. Ream, and T.H. Loughlin (1996):

Northern fur seal, Callorrhinus ursinus, predation on juvenile walleye pollock,

Theragra chalcogramma. In Ecology of Juvenile Walleye Pollock, Theragra

chalcogramma, R.D. Brodeur, P.A. Livingston, T.R. Loughlin, and A.B. Hollowed (eds.), NOAA Tech. Report NMFS 126, 167–178.

Spring, S. (1996): Swimming behavior of walleye pollock larvae Theragra chalcogramma in relation to food. Master of Science Thesis, University of Washington,

Seattle, 123 pp.

Springer, A.M., and G.V. Byrd (1989): Seabird dependence on walleye pollock in

the southeastern Bering Sea. In Proceedings of the International Symposium on

the Biology and Management of Walleye Pollock, Alaska Sea Grant, AK-SG89-01.

Springer, A.M., C.P. McRoy, and M.V. Flint (1996): The Bering Sea Green Belt:

shelf-edge processes and ecosystem production. Fish. Oceanogr., 5, 205–223.
102 S.A. Macklin (ed.)

Stabeno, P.J., and R.K. Reed (1992): A major circulation anomaly in the western

Bering Sea. Geophys. Res. Letters, 19, 1671–1674.

Stabeno, P.J., and R.K. Reed (1994): Circulation in the Bering Sea basin observed

by satellite-tracked drifters: 1986–1993. J. Phys. Oceanogr., 24, 848–854.

Stabeno, P.J., J.D. Schumacher, R.F. Davis, and J.M. Napp. Under-ice observations of water column temperature, salinity and spring phytoplankton dynamics:

Eastern Bering Sea shelf, 1995. J. Mar. Res. (in press c).

Stabeno, P.J., J.D. Schumacher, K. Ohtani, and S. Gladychev. Overview of the

Bering Sea. In The Bering Sea: Physical, Chemical, and Biological Dynamics,

T.R. Loughlin, and K. Ohtani (eds.), Alaska Sea Grant Press (in press a).

Stabeno, P.J., J.D. Schumacher, S.A. Salo, G.L. Hunt Jr., and M. Flint. The

Pribilof Islands: Physical environment. In The Bering Sea: Physical, Chemical,

and Biological Dynamics, Loughlin, T.R., and K. Ohtani (eds.), Alaska Sea

Grant Press (in press b).

Theilacker, G.H., K.M. Bailey, M.F. Canino, and S.M. Porter (1996): Variations

in larval walleye pollock feeding and condtion: A synthesis. Fish. Oceanogr., 5

(suppl. 1), 112–123.

Townsend, D.W., L.M. Cammen, P.M. Holligan, D.E. Campbell, and N.R. Pettigrew (1994): Causes and consequences of variability in the timing of spring

phytoplankton blooms. Deep-Sea Res., 41, 747–765.

Trenberth, K.E., and J.W. Hurrell (1995): Decadal coupled atmosphere-ocean variations in the North Pacific Ocean. Can. Spec. Publ. Fish. Aquat. Sci., 121,

15–24.

VanMeurs, P., and P.J. Stabeno. Evidence of episodic onshelf flow in the southeast

Bering Sea. J. Geophys. Res. (in press).

Vidal, J., and S.L. Smith (1986): Biomass, growth, and development of populations

of herbivorous zooplankton in the southeastern Bering Sea during spring. DeepSea Res., 33, 523–556.

Walsh, J.J., and C.P. McRoy (1986): Ecosystem analysis in the southeastern Bering

Sea. Cont. Shelf. Res., 5, 259–288.

Wyllie-Echeverria, T. (1995a): Sea-ice conditions and the distribution of walleye

pollock (Theragra chalcogramma) on the Bering and Chukchi Sea Shelf. Can.

Spec. Pub. Fish. Aquat. Sci., 121, 131–136.

Wyllie-Echeverria, T. (1995b): Seasonal sea ice, the cold pool and gadid distribution

on the Bering Sea shelf. Ph.D. Dissertation, University of Alaska, Fairbanks,

281 pp.

Wyllie-Echeverria, T., and W.S. Wooster. Year-to-year variations in Bering Sea ice

cover and some consequences for fish distribution. Fish. Oceanogr. (submitted).
Bering Sea FOCI Final Report 103

Part 3A

Juvenile pollock studies (R.D. Brodeur1)

Summary

Analysis of summer survey data from several years indicate that age-0 pollock are more likely to be found in the waters surrounding the Pribilof Islands

than the Bering Sea shelf in general and this area may represent an important nursery ground for juvenile pollock. The frontal zones that surround

each island exhibit elevated levels of phytoplankton and small zooplankton

compared to those found on either side of the front. Acoustic and trawl

catch data show that age-0 pollock are concentrated at these fronts, as are

many piscivorous fishes, seabirds, and marine mammals. Age-0 pollock and

large jellyfish dominate by number and biomass, respectively, the catches

of midwater trawls in the Pribilof Island area. In situ videos have demonstrated that these age-0 pollock are found in the same layer as the jellyfish

during the day and are found to actually associate with these medusae, perhaps to gain protection from visual predators during the day. Age-0 pollock

were larger offshore of the fronts, but an analysis of otoliths of these fish

indicates that the offshore fish are older, suggesting an ontogenetic offshore

movement. Analysis of hatch-date distributions suggests that the Pribilof

fish were spawned on the southeastern Bering Sea shelf and slope. No indication was found of any size-selective predation on age-0 pollock by older

age classes of pollock or other fish predators in any region, although fish predation overall was much greater offshore of the front due to high abundances

of adult pollock in this region.

Summer Distribution of Age-0 Pollock on the

Eastern Bering Sea Shelf

Pelagic trawling was done in 1995 and 1996 aboard a Japanese research vessel

to study the mid-summer distribution of age-0 pollock and associated taxa.

A similar set of grid stations was sampled both years using a rectangular

fine-mesh beam trawl. Bottom temperatures in the Pribilof Island area

were mostly between 3◦ and 4◦C in 1995 and between 4◦ and 5◦C in 1996.

Thermocline depth was centered near 30 m depth in 1995 and around 40 m

in 1996. In both years, standardized catches of age-0 walleye pollock, based

on rough counts at sea, were the highest in the northwest part of the grid

and in the area closest to the Pribilof Islands (Fig. 3A.1). The catch of

juvenile walleye pollock in 1996 was over five times greater than in 1995.

Relatively fewer fish were caught in the southern and eastern portions of the

grid. Noticeably larger age-0 walleye pollock tended to occur in the eastern

part of the survey area, although the actual length measurements will not be

available until the 1996 samples are processed. Larvae of Greenland turbot

1Alaska Fisheries Science Center, NOAA, Seattle, WA 98115, U.S.A.
104 S.A. Macklin (ed.) Figure 3A.1: Location of stations sampled in 1995 and 1996 by the Oshoro Maru for age-0 walleye pollock. The relative size of the dots correspond to the density of age-0 pollock according to the legend.
Bering Sea FOCI Final Report 105

(Reinhardtius hippoglossoides), a common circum-arctic flatfish species, were

frequently collected in 1995 beam trawl samples but were absent from 1996

samples.

There were also some interannual differences in the zooplankton collected

during the 2 years. Both densities and biomass were much higher in 1996

than in 1995. Gelatinous zooplankton (chaetognaths and cnidarians) were

predominant during 1995 whereas euphausiids dominated the 1996 invertebrate catches. In fact, five of the top seven most abundant species collected

in 1996 were euphausiids. There were day/night differences in the catches

of most crustaceans but not of the gelatinous zooplankton.

Distribution and Species Associations of Juvenile

Pollock and Forage Fishes

This project analyzed archival data on abundance and distribution of juvenile pollock and other important forage fishes in the Bering Sea. Forage fish are currently a topic of active research due to recent declines of

marine mammal and seabird populations which have historically depended

upon them. At the “International Symposium of the Role of Forage Fish in

Marine Ecosystems” held in 1996, many of our findings of this project were

presented. This project allowed collaborative research with the Russian fisheries laboratory (TINRO) in Vladivostok whereby a Russian scientist was

able to bring data from the western Bering Sea to Seattle and analyze it

using similar analytical methods for both the eastern and western data sets.

Our study is the first to examine the large-scale distribution patterns

of juvenile pollock and several dominant forage fish species throughout the

Bering Sea. We analyzed new data on the association of these forage fishes

with other taxa that may compete with these forage fishes and, in some

cases, prey upon them. In this study, we examined survey data on some

dominant pelagic forage fishes (herring Clupea pallasi and capelin Mallotus villosus) and the juvenile stages of major commercial groundfish species

(walleye pollock and Pacific cod Gadus macrocephalus). Age-0 pollock had

the highest biomass and were the most widely distributed forage fish on the

eastern Bering Sea shelf (Fig. 3A.2), although jellyfish and age-2+ pollock

dominated the biomass overall. Several geographically distinct assemblages

were recognized in both the eastern and western Bering Sea. Age-0 pollock

were associated with warmer bottom temperatures and capelin with colder

bottom temperatures compared with other species.

Habitat Characteristics of Juvenile Pollock in the

Eastern Bering Sea

Data from a midwater trawl survey of the eastern Bering Sea shelf and

southern Bering Sea basin conducted in 1987 aboard the Russian research

vessel Darwin was analyzed in detail to study the spatial relationships of

juvenile pollock to other pelagic species and to begin to address how these
106 S.A. Macklin (ed.) Figure 3A.2: Distributions of (a) age-0 and (b) age-1 walleye pollock, (c) Pacific herring, and (d) capelin, in the Bering Sea, based on 1987 surveys by Russian research vessels.
Bering Sea FOCI Final Report 107

Figure 3A.3: Age-0 walleye pollock densities and the locations of four different taxonomic groups based

on (top) catch composition and (bottom) optimal habitat of age-0 pollock based on optimal bottom depth,

temperature, and dissolved oxygen, and salinity at 45 m depth. It was found that these were the combination

of variables that were significantly associated with age-0 pollock distribution.
108 S.A. Macklin (ed.)

fish may respond to environmental variability. The availability of pollock

length data made it possible to study the juveniles separately from the

adults. Catch composition and hydrographic data (temperature, salinity,

and dissolved oxygen) were collected during this survey making both a community and a single species approach possible. A synecological approach was

first used assuming that an ordination of the ecological amplitudes of the

various taxa collected may more effectively reflect influential environmental

gradients than considering taxa singly. Cluster and ordination techniques,

incorporating environmental constraints, revealed four bio-types and several

prominent environmental gradients. A basin group and three major shelf

groups were identified as having distinct catch compositions, environmental attributes, and geographic locations (Fig. 3A.3). Juvenile pollock were

mostly found on the shelf. The principle environmental gradients were salinity and dissolved oxygen; temperature was less important. Juvenile pollock

were intermediate in position along these gradients but differences between

age-0 and age-1 cohorts were apparent.

Distribution of Juvenile Pollock and Other Biota

in Relation to Fronts

Using midwater trawl observations from September 1994 and 1995, the abundance, distribution, and size composition of age-0 walleye pollock were examined in relation to the physical oceanography and biology of the structural

front along a transect north of St. Paul Island (Fig. 3A.4). The frontal

region occurred 12–20 km offshore in both years, but the thermocline was

much shallower in 1995 (25 m) than in 1994 (45 m). The isothermal (<8◦C)

inner domain had low chlorophyll, and relatively low small (>153 μm) and

large (>505 μm) fraction zooplankton concentrations. The highest chlorophyll and small zooplankton concentrations occurred at the front and were

lower both inshore and farther offshore of the front. Large zooplankton

(mainly euphausiids and cnidarians) were most abundant in the stratified

offshore waters. By number, age-0 walleye pollock dominated the catches of

midwater trawls (>99% and >95% in 1994 and 1995, respectively). Overall,

however, large medusae dominated the total biomass. Age-0 walleye pollock

densities were the highest at the front or inshore of the front. Age-0 pollock

densities averaged about three times higher in 1994 than in 1995. Age-0

pollock were significantly smaller in 1994 inshore and at the front (mean =

43.4 and 44.6 mm, respectively) than in 1995 (52.2 and 51.7 mm; Fig. 3A.5).

Commensal Associations of Juvenile Pollock with

Schyphomedusae

In September 1995, dense aggregations of large scyphomedusae (mainly

Chrysaora melanaster and Cyanea capillata) were observed in 27 midwater

deployments of a remotely operated vehicle (ROV) near the Pribilof Islands

in the Bering Sea. Age-0 walleye pollock appeared to be frequently associ-
Bering Sea FOCI Final Report 109

Figure 3A.4: (top) Location of sampling transects around the Pribilof Islands, (middle) cross-shelf section of

temperature and identification of different habitats, and (bottom) acoustic backscatter, in the three different

habitats along Transect A in 1994.
110 S.A. Macklin (ed.)

Figure 3A.5: Size distributions of age-0 pollock in the three habitats during 1994 and 1995.
Bering Sea FOCI Final Report 111 Figure 3A.6: (Open boxes) day and (shaded boxes) night differences in the vertical distribution of age-0 pollock and the dominant jellyfish (Chrysaora spp.) alone and found together based on in situ ROV observations made during 1995 around the Pribilof Islands. The number of observations of each occurrence are listed at the bottom of the figure.
112 S.A. Macklin (ed.)

ated with these gelatinous zooplankton. During daytime, up to 30 pollock

were observed swimming within the tentacles of these medusae, but when

approached by the ROV, the pollock generally left the vicinity of the jellyfish.

At night, few such associations were observed and juvenile pollock moved

closer to the surface (Fig. 3A.6), apparently feeding in loose aggregations,

while the medusae remained close to the thermocline (35–40 m). Trawl collections during the day showed a strong association between age-0 pollock

and medusae density, whereas at night no such association was observed.

The lack of gelatinous material in the stomachs of the pollock suggests that

juvenile pollock associate to gain shelter from predation. This commensal

behavior with gelatinous zooplankton may have important implications relevant to pollock recruitment dynamics in the Eastern Bering Sea if these

juvenile pollock substantially decrease their vulnerability to predation by

seeking shelter within jellyfish tentacles.

Variability in Feeding and Condition of Age-0

Pollock in Relation to Fronts

Dietary composition, feeding intensity, and condition index of age-0 walleye

pollock were examined for variations related to time of day, location, size

of predator, and year. Stomach contents of pollock collected at a hydrographic front near the Pribilof Islands during September 1994 through 1996

were compared with those from pollock collected on either side of the front.

Diets were dominated in all three regions by small zooplankton, mainly copepods, pteropods, euphausiids, and chaetognaths, but fish and some epibenthic crustaceans were also consumed. Copepods and pteropods dominated

the diet in all years and areas by number but the diet was more mixed by

weight with chaetognaths, euphausiids, and fish (smaller pollock) also being

important (Fig. 3A.7). Copepods were more abundant in the diet during the

day. No significant day/night differences in weight composition were noted.

Stomach fullness was highly variable by year and habitat and no significant

differences were observed. Stomach fullness peaked at around sunset for fish

<50 mm and at night for the larger fish, implying that feeding chronology

changed with ontogeny. Age-0 pollock condition factor (Fulton’s K) varied

from 0.45 to 1.20 (mean = 0.767 ± 0.09 (SD)). Year was not found to be an

important factor in determining condition although location with respect to

the front was important.

Age and Growth of Juvenile Pollock in Relation to

the Fronts

The hatch-date distributions for the fish taken at ten stations in the 1994

sampling area showed that hatching occurred from mid April through early

July with a peak occurring in June. Allowing approximately 1 month from

spawning to hatching, at water temperatures of 1–3◦C, it can be presumed

that these fish were spawned from late March through early June with a
Bering Sea FOCI Final Report 113

Figure 3A.7: Interannual and habitat differences in the percentage weight composition of the diet of age-0

pollock on Transect A north of St. Paul Island. Stomach contents are grouped into major prey categories.

The number of stomachs examined in each category is given at the top of each figure.
114 S.A. Macklin (ed.) Figure 3A.8: Hatch-date distributions of age-0 walleye pollock collected around the Pribilof Islands during September 1994.
Bering Sea FOCI Final Report 115

peak in spawning during May. This spawning period coincides with the

spawning period for pollock on the southeastern continental shelf and slope

of the Bering Sea. Age in days after hatching ranged from 76 to 152 and was

predominantly less than 120 days (Fig. 3A.8). Some geographical distinction

is noticeable in the age-length relationship, particularly among the larger

fish. The possibility of variability in growth rates was investigated using

growth among individual fish backcalculated using otolith microincrement

measurements. Even though sampling was limited at and inshore of the

tidal fronts around the Pribilof Islands, it seems from the data that fish

were smaller and younger at these locations than those sampled offshore of

the fronts.

Covariation of Plankton, Juvenile Fish, and

Seabirds at Tidal Fronts

Tidally generated shelf frontal systems around the Pribilof Islands offer a

unique setting where the effects of ocean dynamics on the production and

distribution of plankton, nekton, and seabirds can be observed. During a pilot study in late summer 1994, the frontal zone between inshore and offshore

regimes northeast of St. Paul Island was sampled by continuous underway

transects of hydroacoustics (38, 120, and 200 kHz) and seabird counts to determine the distributions of juvenile fish and their predators. Net sampling

of juvenile fish and their planktonic prey followed. Echograms of volume

backscatter (Sv) at all frequencies showed a correspondence between scatterer density and hydrography. By rendering differences in volume backscatter (Fig. 3A.9) at two frequencies as echograms (Sv200–Sv120), we were able to

discriminate between layers of fish (with or without zooplankton) and layers

of zooplankton (without fish). Juvenile walleye pollock comprised >90% of

fish biomass captured with a pelagic trawl. The dominant zooplankton scatterers had different vertical distribution patterns in different hydrographic

regimes (inshore, frontal, and offshore). In the offshore regime, fish were

aggregated around the thermocline (ca. 40 m) during the day, and migrated

to the surface at night. Biomass of large zooplankton was highest in this

regime (250 ml m−3), and some of the potential prey populations remained

below the thermocline at night after the distribution of fish shoaled. Juvenile walleye pollock were more abundant in the front (>200–1000 m−3) than

either of the other regimes. Biomass of small zooplankton was highest in

the frontal zone (>700 ml m−3). Seabirds (murres, Uria spp.), whose diet is

strongly dependent on the availability of juvenile fish, were most abundant

just offshore of, rather than in, the front.

Predation on Juvenile Pollock by Major Teleost

Predators

Spatial and temporal variation in the consumption of age-0 walleye pollock

by arrowtooth flounder (Atherethes stomias) and older age classes of pollock
116 S.A. Macklin (ed.)

Figure 3A.9: Acoustic backscatter difference between 120 kHz and 200 kHz during the (top) day and

(bottom) night along Transect A in 1994. Note the layering of what is apparently zooplankton at the

thermocline around 40 m.
Bering Sea FOCI Final Report 117 Figure 3A.10: Diet composition of age-1 and adult pollock at the front and offshore by major prey.
118 S.A. Macklin (ed.)

was examined at the tidal front located north of St. Paul Island, Alaska. Age0 walleye pollock were the primary prey of arrowtooth flounder throughout

the day, but were least digested in the late day, indicating a diurnal feeding

pattern. A similar diurnal pattern was not seen in the vertical distribution

of age-0 walleye pollock, suggesting that the feeding pattern exhibited by

arrowtooth flounder was based upon their migratory behavior. Lengths of

age-0 walleye pollock consumed by arrowtooth flounder were similar to those

sampled from mid-water trawls. Walleye pollock cannibalism was examined

along a transect that included samples collected at the front and offshore

of the front. Age-0 walleye pollock were the primary prey (by weight) of

walleye pollock at all locations (Fig. 3A.10). Adjacent cohort cannibalism

was prevalent (age-0 walleye pollock were 79% of the diet by weight) at the

frontal region. Age-0 walleye pollock cannibalism removal estimates were

highest at the front for age-1 walleye pollock and offshore for the adults.

The much higher removal rate of age-0 by age-1 walleye pollock at the front

compared to the offshore region is due to an order of magnitude larger predator biomass at the front and nearly double the percent by weight of age-0

walleye pollock in the diet. Adults cannibalizing age-0 walleye pollock at a

much higher rate offshore than at the front is also a result of higher adult

walleye pollock biomass offshore than at the front. Prey selectivity analysis

indicated that age-0 walleye pollock were more highly selected offshore than

at the front.

Seabird Distributions Relative to Frontal Regions

Data on the distribution and abundance of seabirds were collected in 1994

aboard the R/V Surveyor (950 nautical miles surveyed), in 1995 aboard the

Surveyor (250 nm) and R/V Miller Freeman (230 nm), and in 1996 aboard

Miller Freeman (135 nm). Continuous counts of birds were made from the

flying bridge while the ship was underway and all birds within an arc from

300 m ahead of ship to 90◦ off the port side were recorded using a standard

strip transect method.

Murres (Uria lomvia and U. aalge) and puffins (Fratercula cirrhata and

F. corniculata), whose diets consist of primarily juvenile pollock, breed in

large numbers on the Pribilof Islands. High concentrations of murres foraged

on the seaward edge of the front north of St. Paul Island. Murres were

observed in these stratified waters in 1994 and 1995. In particular, the

abundance of feeding murres was greatest in 1995 over stratified water 30

to 42 km north of St. Paul Island where acoustic sign was dense and close

to the surface. South of St. Paul Island, relatively large numbers of feeding

murres were found in the transition zone between stratified and mixed water.

In addition to the area north of St. Paul Island, consistent aggregations of

foraging piscivores were also observed along the first 12–15 km south of St.

George Island. Murres and puffins were relatively abundant in the inshore,

vertically mixed waters south of St. George in the fall of 1995, as was the case

for murres in 1996 (Fig. 3A.11). North of St. George, murres and puffins

were relatively abundant nearshore over a shallow (∼25 m) pycnocline in
Bering Sea FOCI Final Report 119

Figure 3A.11: The density of foraging murres observed on Line A (top) north of St. Paul Island. No more

than 2.2 murres km−2 were observed on Line A in 1996; therefore, these observations were omitted. The

density of foraging murres observed on Line D (bottom), south of St. George Island. Comparable area not

sampled in 1994.
120 S.A. Macklin (ed.)

1996. Perhaps vertical mixing enhances production here and thus foraging

birds are attracted to this location. Farther offshore during this same cruise,

the depth of the pycnocline increased to 50 m and the pycnocline was no

longer apparent at the northern end of the line. Despite the presence of

dense acoustic sign near the Pribilof Canyon, we observed very few murres

and puffins feeding in this location.

Fur Seal Distributions Relative to Frontal Regions

Marine mammal observations were conducted in 1994–96 from the flying

bridge during daylight hours when the vessel was underway. Transects and

ship movements were designed for oceanographic and trawling effort, so marine mammal observations were opportunistic and not conducted for abundance estimates. In 1995 and 1996, shipboard survey efforts were coordinated with concurrent studies on female fur seal movements using satellite

telemetry. The vessel detoured for special prey trawling effort in areas of

high fur seal density, as indicated by shipboard observations and satellite

records.

The overall number of marine mammal sightings was quite low (n =

273). However, a preliminary analysis indicates that the highest density of

fur seals sighted from the ship corroborate satellite records of female movement patterns during feeding bouts, and generalized areas of high pollock

density. The greatest number of on-effort hours and the greatest number of

sightings per unit effort were in 1995. In October of 1995, satellite tracked

female fur seals from St. Paul Island concentrated their foraging efforts to

the north and northwest of St. Paul Island. Fur seal females tracked from

St. George Island foraged south of St. George Island exclusively. These

patterns are very similar to the distribution of fur seals observed from the

ship in September 1995, with the exception that relatively high densities

of seals were also observed along the transect southeast of St. Paul Island

(running between St. Paul and St. George). Correlation between observed

and recorded movements of fur seals in 1996 are currently being analyzed as

well as the larger question of the relationship between fur seal movements

and the concentration of their prey along frontal boundaries.

References

Brodeur, R.D. In situ observations of the association between juvenile fishes and

scyphomedusae in the Bering Sea. Mar. Ecol. Prog. Ser. (in press).

Brodeur, R.D., P.A. Livingston, T.R. Loughlin, and A.B. Hollowed (1996): Ecology

of juvenile walleye pollock, Theragra chalcogramma. NOAA Tech. Rep. NMFS

126, 227 pp.

Brodeur, R.D., M.T. Wilson, and L. Ciannelli. Spatial and temporal variability in

feeding and condition of age-0 walleye pollock in frontal regions of the Bering

Sea. ICES J. Mar. Sci. (submitted).

Brodeur, R.D., M.T. Wilson, J.M. Napp, P.J. Stabeno, and S. Salo (1997): Distribution of juvenile pollock relative to frontal structure near the Pribilof Islands.
Bering Sea FOCI Final Report 121

In Proceedings of Forage Fishes in Marine Ecosystems, Alaska Sea Grant AKSG-97-01.

Brodeur, R.D., M.T. Wilson, G.E. Walters, and I.V. Melnikov. Forage fishes in

the Bering Sea: Distribution, species associations, and biomass trends. In The

Bering Sea: Physical, Chemical, and Biological Dynamics, T.R. Loughlin, and

K. Ohtani (eds.), University of Alaska Sea Grant (in press).

Ciannelli, L., R. Brodeur, and T. Buckley. Development and application of a bioenergetics model for juvenile walleye pollock. J. Fish Biol. (in revision).

Lang, G.M., R.D. Brodeur, J.M. Napp, and R. Schabetsberger. Variation in fish

predation on juvenile walleye pollock relative to hydrographic structure near

the Pribilof Islands, Alaska. ICES J. Mar. Sci. (submitted).

Napp, J.M., R.D. Brodeur, D. Demer, R. Hewitt, P.J. Stabeno, G.L. Hunt, Jr., and

J.D. Schumacher. Observations of nekton, zooplankton, and seabird distributions at tidally generated shelf fronts in the eastern Bering Sea. Mar. Ecol.

Prog. Ser. (submitted).
122 S.A. Macklin (ed.)
Bering Sea FOCI Final Report 123

Part 3B

Modeling the upper ocean production dynamics of

plankton and larval pollock in the Bering Sea

(Stephen M. Bollens1 and Bruce W. Frost2)

Introduction

We constructed and applied a coupled multi-species biological-physical model

to investigate the production dynamics of the pelagic ecosystem in the Bering

Sea, especially in regards to the early life history stages of pollock. In addition, our work focused on assimilating into our model newly generated

physical (e.g., PEGGY) and, to a lesser degree, biological (e.g., zooplankton) field observations. We then used this model and data to address several

key questions regarding how and why different processes—namely, protozoan dynamics, short-term mixed layer depth variability, and species-specific

copepod dynamics—affect growth of larval pollock on the shelf of the southeastern Bering Sea. This work will continue to aid the BS FOCI and the

SEBSCC programs in identifying specific hypotheses to be tested in the field

and laboratory, as well as generally lead to a better understanding of how

and why variable physical and biological processes regulate dynamics of biological production in upper ocean ecosystems. This latter point has obvious

implications for management of the pollock fishery in the Bering Sea, as

discussed below.

Background

The eastern Bering Sea can be divided into four distinct oceanographic domains (Coachman, 1986). For the purposes of the current discussion, we focus on the deep (>3500 m) open basin and the mid-continental shelf. These

two domains differ dramatically in both physical (e.g., Coachman, 1986) and

biological (e.g., Smith and Vidal, 1986) oceanographic dynamics. In a general sense, different planktonic production dynamics in each domain would

be expected to result in different levels of production of larval fish, with

copepods and other zooplankton acting as “filters” of primary production

(Runge, 1988). However, while such a linkage between larval fish production

and lower-level planktonic production in the Bering Sea has obvious intuitive

appeal, the exact nature of this linkage, and the role played by site-specific

physical processes in regulating it, have yet to be determined. This was the

fundamental problem we wished to address with the proposed research.

1San Francisco State University, California

2University of Washington, Seattle
124 S.A. Macklin (ed.)

Results

Model Construction and Elaboration

We have adapted the nutrient-phytoplankton-zooplankton model of Frost

(1987) to include stage-structured dynamics of copepod populations and

growth of larval pollock as a function of abundance of appropriately sized

prey. Input data were taken from the Bering Sea (e.g., the PROBES study

and other historical data) whenever possible, but were at other times taken

from Ocean Station Papa in the North Pacific, as described below. Model

output consists of daily concentrations of nutrient, phytoplankton, and all

developmental stages of copepods, as well as growth rate of larval pollock.

Protozoan microplankton and dynamically modeled mixed-layer depths were

also added to the model as described below.

The dynamics of phytoplankton (P) in the mixed layer is modeled using the equation of Frost (1987) modified to include two types of grazers,

a population of protistan herbivorous microzooplankton (M) and a stagestructured population of suspension feeding copepods (Cj ):

dP

dt = 1zm

zm

0

P(PMAX) tanh  αP ARz

ψPMAX 

− rp(PMAX)P

 N

d + N

−eM(P − P0)M

fM + P − P0

−  ec(P + M − P0)

fc + P + M − P0

CjW0.75

j + v (Pzm+1 − P)

where

PMAX =



eD ln 2 − 1.0



DL/24,

with

D = doublings d−1 = 0.851 

100.02750and DL = day length,

and

P ARz = 0.5Iz = I0e−kz,

where I0 is daily incident solar radiation, z is depth, and k is the attenuation

coefficient for irradiance. It is assumed that irradiance is absorbed by both

the water and phytoplankton; thus k = aP y−1+b{a = 0.02 m2 (mg Chla)−1

and b = 0.1 m−1}. All other variables and parameters are defined in Table 3B.1. Phytoplankton production is integrated over the mixed layer (zm),

and then homogenized to calculate the change in phytoplankton stock due

to production, grazing, and mixing. A constant phytoplankton carbon-tochlorophyll a ratio (y) was assumed. Grazing mortality of the phytoplankton

is due to both microzooplankton and copepods.

The dynamics of herbivorous protistan microzooplankton is described as:

dM

dt = M (aM − rM) eM (P − P0)fM + P − P0

− gM (M − M0)

hM + M − M0

M + v (Mzm+1 − M)

It is assumed that the source(s) of predation mortality is not exclusively due

to copepod ingestion, and thus mortality is parameterized with a MichaelisMenten function. Also, microzooplankton behave as passively mixed particles (the third term).
Bering Sea FOCI Final Report 125

Table 3B.1: Multi-species model variables and standard values.

Parameter description [units]

Physical Environment

maximum mixed-layer depth (MLD) [m] 75

time of initial MLD shoaling [julian day] 90

minimum MLD [m] 30

time of initial minimum MLD [julian day] 135

minimum temperature [◦C] 0

maximum temperature [◦C] 8

mixing rate (ν) [d−1] .01

Phytoplankton Diatoms Dinoflagellates

initial nitrate concentration N(t=0) [mM m−3] 10.8 10.8

intial chlorophyll concentration P(t=0)ψ−1

[mg chla m−3] .15 .15

carbon:chlorophyll (ψ) [mgC (mg chla)

−1] 30 30

half-saturation of N uptake (d) [mM m−3] 1.0 1.0

photosynthetic efficiency (α)

[mgC (mg chla)

−1 ly−1] 1.0 1.0

maximum doublings per day (@10◦C) [D] 1.6 1.6

respiration as % phytosynthesis [rP ] .10 .10

Protozoa

initial biomass M(t=0) [mgC m−3] 2.45

maximum ingestion rate (eM) [d−1] .728

half-saturation ingestion (fM ) [mgC m−3] 20

feeding threshhold (p0) [mgC m−3] 10

respiration as % of grazing (rM) .40

assimilation efficiency (aM) 0.8

maximum mortality rate (gM) [d−1] .80

half-saturation of mortality (hM ) [mgC m−3] 50

Copepods Calanus Neocalanus Pseudocalanus Metridia

initial biomass C(t=0) [mgC m−3] .0238 .26 .0238 .26

time of initial biomass [julian day] 90 30 30 30

period of introduction to the surface [days] 1 60 1 1

maximum ingestion rate (eC) [d−1] 1.25 .55 .75 1.5

half-saturation of ingestion (fC ) [mgC m−3] 50 50 25 50

feeding threshhold (P0) [mgC m−3] 10 10 5 10

respiration as % of grazing (rC) .40 .40 .40 .40

assimilation efficiency (aC) 0.8 0.8 0.8 0.8

maximum mortality rate (gC ) [d−1] .10 .10 .10 .10

half-saturation of mortality (hC ) [mgC m−3] 1000 1000 1000 1000

minimum egg development time [days] 4 4 4 4

female:male to recruits 0.8 0.8 0.8 0.8

power dependence of weight on growth 0.75 0.75 0.75 0.75

egg weight [μgC] 0.25 1.0 .08 0.1

adult weight [μgC] 100 416 8 55

Larval Pollock

maximum ingestion rate (eF ) [d−1] 1.35

half-saturation of ingestion (fF ) [mgC m−3] 19

intial larval weight [μgC] 140

maximum size of food as % of larval weight 4

power dependence of weight on growth 0.75
126 S.A. Macklin (ed.)

The dynamics of copepod populations are simulated as the production

of daily cohorts of eggs, and the subsequent changes in numbers and masses

of individuals in those daily cohorts (e.g., Steele and Frost, 1977). The

production of cohorts of eggs on day j was determined by the growth rate

of adult female copepods:

Cj (t = 0) = Cad

(aC − rc) ec (P + M − P0)

fc + P + M − P0

W0.75

ad 

/W(t = 0)

where the summation is over 1 day for the broadcast spawner. The initial

individual mass on day j [W(t = 0)] is the mass of the egg. It is assumed

that copepods feed indiscriminately on phytoplankton and protistan microzooplankton. The subsequent change in individual mass (Wj ) and numbers

(Cj ) in cohort j are described as:

dWj

dt = (aC − rc) ec (P + M − P0)fc + P + M − P0

W0.75

j

dCj

dt = gcCjhc + Cj

Cj

Predation closure of the model is parameterized as a Michaelis-Menten function without a threshold abundance since it is assumed that larval fish do

not significantly impact their prey populations. It was assumed that the

copepods maintain their abundances in the mixed layer through vertical migration. That is, as the mixed-layer shoals, the concentration of copepods

in the mixed-layer increases, and similarly decreases with mixed-layer deepening, thus conserving the actual number of animals in the mixed-layer.

Dissolved nitrogenous nutrient is described as:

dN

dt = −ξzm

zm

0

P(PMAX) tanh  αP ARz

cPMAX 

− rp(PMAX)P

 N

d + N

+ ξ

rMeM(P − P0)M

fM + P − P0

+ ξ

 rzec(P + M − P0)

fc + P + M − P0

CjWj + v (Nzm+1 − N)

Where the first term represents the photosynthetic utilization of nitrate.

A constant nitrogen-to-carbon ratio (x) is used to convert phytoplankton

carbon uptake rate to an equivalent rate of nitrogen utilization. The second

and third terms describe the nitrogen reintroduced into the system due to

microzooplankton and copepod respiration. Finally, sub-mixed-layer nitrate

(Nzm+1) mixed (diffused) into the mixed layer.

Growth rate of larval pollock was modeled as a function of availability of

copepod prey biomass (CjWj ), including eggs, in the appropriate size range

(j,k) and protozoan biomass (M):

dF

dt =

0.3eF







k

j

CjWj + M





fF +







k

j

CjWj + M




Bering Sea FOCI Final Report 127

Each model is initialized with a standing stock concentration of phytoplankton (P) and protozoa (M). An initial biomass of adult female Calanus

appear in the surface water in early spring over a period of 1 day. Neocalanus, on the other hand, is initialized as C1 copepodites appearing in the

surface waters over a period of 2 months starting in mid-winter. Note the

food web structure was simplified by initializing protozoa abundance to zero.

The physical characteristics of the basin and midshelf environment were

simulated using idealized mean seasonal mixed-layer depths (Zm), temperatures (T), and solar insolation (Io). Wintertime conditions in the Bering Sea

result in deep mixed-layer depths (150 m) in the basin (Dodimead, 1963);

whereas Zm of the shelf is limited by the depth of the bottom (75 m). Due

to solar heating and decreasing winds, mixed-layer depths in both regions

shoal in (the late) spring.

To evaluate the effect of daily mixed-layer depth variability on the food

web dynamics, daily mixed-layer depth was simulated using the Price et al.

(1986) mixed-layer model (PWP). The model has been successfully used to

model daily mixed-layer variability in a variety of regions (e.g., Davis and

Steele, 1994). Given the limited pertinent observations in the Bering Sea,

the physical model was forced using representative meteorological data (i.e.,

1977) from Ocean Station Papa in the north Pacific (50◦N, 145◦W). The

initial subsurface density structure was prescribed to simulate mixed-layer

depth and temperature in the Bering Sea (Dodimead et al., 1963; Favorite

et al., 1976). The resulting daily mixed-layer depths were then used to force

the biological model described above. Since this version of the biological

model is limited to two layers, and thus the subsurface structure is poorly

resolved, we have constrained the model not to dilute the passive constituents

(e.g., phytoplankton and protozoa) with rapid deepening of the mixed layer

(otherwise extreme and unrealistic dilution occurs).

We recently extended this model to include stage-structured dynamics

of four copepod populations (Calanus, Pseudocalanus, Metridia, and Neocalanus), two functional groups of phytoplankton (diatoms and dinoflagellates), and larval pollock feeding and growth. Model variables and standard

values for the multi-species model are given in Table 3B.1. This extended

model was for the most part driven by extremely simplified physical oceanographic dynamics, with the water column consisting of two layers (mixed

layer and deep layer), and exchange between layers occurring as a result of

mixed layer shoaling/deepening (detrainment/entrainment) and turbulent

vertical mixing. Model output consists of simulated daily abundances of

nitrogenous nutrients, diatoms, dinoflagellates, protistan microzooplankton,

copepod developmental stages of each of four species, sizes (weight) of larval

pollock, and instantaneous growth rates of larval pollock.

Model Results-Generic Seasonal Cycles

Early model results highlight several important phenomena. (Note that

these results have appeared elsewhere, i.e., numerous presentations at scientific meetings and previous annual reports, as well as manuscripts soon

to be published (e.g., Francis et al., in press; Bollens et al., in prepara-
128 S.A. Macklin (ed.)

tion). What follows is only a very brief summary of these results). First

is the species composition and dynamics of meso/macrozooplankton: larval

pollock dependent on Calanus (e.g., on the shelf) should experience much

better growth conditions later in the spring, whereas those dependent on

Neocalanus (e.g., in the deep basin) are likely to grow more slowly, generally,

although somewhat better earlier in the year when young Neocalanus are

first recruited to the surface layer. Second is the role of protozoans: larval

pollock in this model are highly dependent on these organisms for sustaining high growth rates, especially during times of year when young copepods

are not abundant (i.e., early spring on the shelf and late spring/summer in

the basin). A third process, short-term mixed-layer depth variability, has

significant impacts on lower trophic levels (phytoplankton and protozoans)

but less effect on copepods and larval pollock growth rate. We are in the

process of examining this last point in much greater detail by fully coupling

our biological model to the Price-Weller-Pinkel mixed-layer physical model

(Price et al., 1986).

These modeling results point to several data gaps and processes/

phenomena that need to be addressed through further modeling, field, and

laboratory studies. The first is the functional response of larval pollock (ingestion vs. prey concentration), the parameterization of which could only

be crudely approximated in this study, but to which the model is very sensitive. Second is the distribution and abundance of protozoans (of which

we know virtually nothing in the Bering Sea) and the degree to which these

organisms provide nutrition for larval pollock. Third is the field collection of

time series data on basic biological, physical, and meteorological variables,

especially early in the year (winter/early-spring).

Multi-Species Model and Assimilation of 1992–1994 Physical

Oceanographic Data

Results of the multi-species model—including the dynamics of Calanus,

Pseudocalanus, Metridia, and Neocalanus, as well as two functional groups

of phytoplankton (diatoms and dinoflagellates), and larval pollock feeding

and growth rates—need to be evaluated in light of recent field data on zooplankton abundance and composition. (Note: these field data, from the

1992–1994 field seasons, were only made available to us in September 1997).

Nevertheless, preliminary model results (Fig. 3B.1) indicate that there are

significant differences in the dynamics of the main mesozooplankton taxa,

and that Metridia may in particular be a key link between primary producers

and larval pollock growth rate. More work is needed in this area, however.

We have also run the multi-species model using the physical oceanographic data collected by the PEGGY mooring during 1992–1994 (Figs. 3B.2–

4). Clear differences are evident between years. For instance, larval pollock

growth rate is very low in late June of 1993 (0.03–0.06 per day) compared

with rates predicted for either 1992 or 1994 (0.12–0.15 per day). This low

rate of growth seems to be due to the rapid deepening of the mixed layer in

1993, and would be expected to have the effect of diluting concentrations of
Bering Sea FOCI Final Report 129

Figure 3B.1: Multi-species plankton—larval fish model on the shelf.
130 S.A. Macklin (ed.)

Figure 3B.2: Multi-species plankton—larval fish model on the shelf, 1992.
Bering Sea FOCI Final Report 131

Figure 3B.3: Multi-species plankton—larval fish model on the shelf, 1993.
132 S.A. Macklin (ed.)

Figure 3B.4: Multi-species plankton—larval fish model on the shelf, 1994.
Bering Sea FOCI Final Report 133

larval pollock prey (nauplii and protozoans). Here too more work is needed

to fully assimilate the field data and otherwise validate the model.

Future Activities and Anticipated Milestones

We plan to continue our modeling work with emphasis on data assimilation from the 1992, 1993, and 1994 field studies (particularly zooplankton

data and physical and meteorological data from the PEGGY moorings). We

anticipate producing one or more manuscripts detailing the results of our

multi-species model and data assimilation for publication in Marine Ecology Progress Series, Fisheries Oceanography, Journal of Marine Science, or

related peer-reviewed journal; submission of such manuscript(s) would be

expected in late 1997 or early 1998.

Management Implications

As noted above, this work will continue to aid current (e.g., SEBSCC) and

future scientific programs in identifying specific hypotheses to be tested in

the field and laboratory. Moreover, our modeling work has led to a better

understanding of how and why variable physical and biological processes regulate dynamics of biological production in upper ocean ecosystems generally,

and the Bering Sea in particular.

This has obvious implications for management of the pollock fishery in

the Bering Sea. For instance, if appropriate physical oceanographic data

could be collected in “real time,” via moorings (e.g., PEGGY) or satellites,

a model such as described above could be implemented and predictions generated of larval pollock growth rate. When coupled with other models concerned with larval mortality and/or juvenile growth and mortality, such a

model could generate predictions of pollock recruitment strength. While

such a series of coupled models may not yet be in hand, it is a very reasonable short-term to medium-term (2–5 yrs.) goal, and would provide managers

another tool with which to manage the Bering Sea pollock fishery.

References

Archer, D., T.M. Powell, and B.W. Frost (1990): Results from a coupled mixed

layer physics-ecosystem process model in the N. Pacific. Eos, Trans. AGU,

71(2), 180.

Bollens, S.M., M.C. Landsteiner, B.W. Frost, K. Bailey, and C.S. Davis. A model

of the upper ocean production dynamics of zooplankton and larval pollock in

the Bering Sea. Mar. Ecol. Prog. Ser. (in preparation).

Coachman, L.K. (1986): Circulation, water masses, and fluxes on the southeastern

Bering Sea shelf. Cont. Shelf Res., 5, 23–108.

Cooney, R.T., and K.O. Coyle (1982): Trophic implications of cross-shelf copepod

distributions in the southeastern Bering Sea. Mar. Biol., 70, 187–196.

Davis, C.S. (1984): Interaction of a copepod population with the mean circulation

on Georges Bank. J. Mar. Res., 42, 573–590.
134 S.A. Macklin (ed.)

Dodimead, A.J., F. Favorite, and T. Hirano (1963): Salmon of the North Pacific

Ocean, Part II: Review of Oceanography of the Subarctic Pacific Region. Int.

North Pac. Fish. Comm. Bull., 13, 195 pp.

Favorite, F., A.J. Dodimead, and K. Nasu (1976): Oceanography of the Subarctic

Pacific Region, 1960–1971. Int. North Pacific Fish. Comm. Bull., 33, 187 pp.

Francis, R.C., R. Merrick, S.M. Bollens, and K. Aydin. Modeling and Management

of the Bering Sea Ecosystem. In The Bering Sea Ecosystem, R.C. Francis (ed.),

University of Washington Press, Seattle (in press).

Frost, B.W. (1982): Modeling effects of environmental perturbations on marine

plankton dynamics. In Second US/USSR Symposium: Biological Aspects of

Pollutant Effects on Marine Organisms, D.J. Baumgartner, and A.I. Siminov

(eds.), U.S. Environmental Protection Agency document EPA-600/3–82–034,

1–15.

Frost, B.W. (1987): Grazing control of phytoplankton stock in the open subarctic

Pacific Ocean: a model assessing the role of mesozooplankton, particularly the

large calanoid copepods, Neocalanus spp. Mar. Ecol. Prog. Ser., 39, 49–68.

Frost, B.W. (1993): A modelling study of the processes regulating plankton standing

stock and production in the subarctic Pacific Ocean. Prog. Oceanogr., 32, 17–

56.

Heinrich, A.K. (1962): The life histories of plankton animals and seasonal cycles of

plankton communities in the oceans. J. Cons. Int. Explor. Mer., 24, 455–464.

Hood, D.W. (1986): Processes and resources of the Bering Sea Shelf (PROBES).

Cont. Shelf Res., 5, 1–288.

Price, J.F., R.A. Weller, and R. Pinkel (1986): Diurnal cycling: observations and

models of the upper ocean response to diurnal heating, cooling, and wind mixing. J. Geophys. Res., 91, 8411–8427.

Runge, J.A. (1988): Should we expect a relationship between primary production

and fisheries? The role of copepod dynamics as a filter of trophic variability.

Hydrobiologia, 167, 61–71.

Smith, S.L., and J. Vidal (1986): Variations in the distribution, abundance, and

development of copepods in the southeastern Bering Sea in 1980 and 1981.

Cont. Shelf Res., 5, 215–239.

Steele, J.H., and B.W. Frost (1977): The structure of plankton communities. Phil.

Trans. Roy. Soc. Lond. B, 280, 485–534.
Bering Sea FOCI Final Report 135

Part 3C

Seasonal sea ice in the Eastern Bering Sea (James

D. Schumacher1 and Tina Wyllie-Echeverria2)

A striking feature of the physical environment of the eastern Bering Sea

is the occurrence of seasonal sea ice. The extent fluctuates over 1000 km

between waters north of the Bering Strait in the summer south to the Alaska

Peninsula and southeastern shelf break in winter. The actual mechanism of

ice formation for the eastern shelf has been described by a “conveyor belt”

analogy (Pease, 1980; Overland and Pease, 1982). Ice is produced along

leeward (south-facing) coasts primarily located in the northern region of the

shelf, and driven by wind to its thermodynamic limit where it melts. As

water freezes brine rejection occurs and the salinity of the ice varies between

5–12 psu. Regions of open water, or polynyas, are created by downwind

advection of ice. The sea ice limit advances southward as ice-melt cools and

freshens the upper ocean. During winter, a climatological average of 3 to

5 storms per month move eastward along the Aleutian Chain forming the

primary storm track, while less than two storms per month cross the northern

Bering Sea. The amount of sea ice production and advection depends upon

which atmospheric conditions dominate in a given winter. The greatest ice

production occurs in years when the Aleutian Low is well developed and

storms migrate along the primary storm track.

For the Bering Sea, variations in overall ice cover (Fig. 3C.1), time of advection over the open shelf, and subsequent melt-back are important features

of the physical environment. Formation of sea ice generally begins in November with maximum ice extent occurring in late March. Ice-free conditions

typically exist from June through October. Observations of ice cover over

the eastern Bering Sea shelf show a nearly 40% variation about the mean

(Niebauer, 1988). Other characteristics of ice cover that show great variability include duration of ice at its southern extent (3–15 weeks), time of retreat

from the southernmost extent (between mid-March and June), and number

of weeks that ice remained over the middle shelf domain (3–28weeks with

a mean of 20 weeks) (Wyllie-Echeverria, 1995b). The differences in these

characteristics vary greatly between years with maximum and minimum ice

extent (Fig. 3C.2).

Ice formation, brine rejection, advection and eventual melting play a critical role in fluxes of heat and salt (Aagaard et al., 1985; Hendricks et al.,

1985; Coachman, 1986) and in generation of baroclinic flow (Schumacher et

al., 1983; Muench and Schumacher, 1985). The production of dense (cold

saline) water has a marked impact on the halocline of the Arctic Ocean with

water from the Anadyr and Anadyr Strait polynyas providing a substantial

fraction of the total (Cavalieri and Martin, 1994). From 9–25 m of ice formation occurs over the winter season depending on location and meteorological

1Pacific Marine Environmental Laboratory, NOAA, Seattle, WA 98115, U.S.A.

2Joint Institute for the Study of the Atmosphere and Ocean (JISAO), University of

Washington, Seattle
136 S.A. Macklin (ed.)

Figure 3C.1: Approximate location of the maximum sea ice extent in a year with extreme ice cover (1976)

and in a year with minimal ice cover (1979).

conditions (Cavalieri and Martin, 1994). A growth rate of ∼6 cm d−1 was

estimated from changes in salinity (Schumacher et al., 1983; Roach et al.,

1995). The average thickness of ice at any given instant over most of the

open southeastern shelf, however, is only ∼0.5 m (Coachman, 1986). The

positive buoyancy flux from melting ice initiates both baroclinic transport

along the marginal ice zone (∼0.3 × 106 m3 s−1) and stratification of the

water column.

Sea ice also exerts an important influence on the biota. Associated with

ice-melt is a bloom of phytoplankton that accounts for 10–65% of the total annual primary production over the eastern shelf (Niebauer et al., 1990,

1995). More recent observations (Stabeno et al., 1998) demonstrate that

chlorophyll concentrations begin to increase concomitant with the presence

of sea ice even though the water column is not stratified. Sea ice plays a

central role in the timing of primary secondary production cycles which can

influence food availability for first feeding pollock larvae. Ice production
Bering Sea FOCI Final Report 137

Figure 3C.2: Characteristics of sea ice extent measured along 169◦W each week for atmospheric conditions

during a cold year (1975–1976: shown as dark line and dots) and a warm year (1978–1979: shown as light

line and dots). Note the differences in time of advance, southern limit, duration over the Middle shelf and

time of retreat (after Wyllie-Echeverria, 1995b).

and formation of cold bottom water (the cold pool) also influences the distributions of higher trophic level biota over the eastern shelf (Ohtani and

Azumaya, 1995; Wyllie-Echeverria, 1995a, b). This latter effect may influence the overlap of young of the year pollock and older fish, thereby providing

a physical determinant for the extent of cannibalism in a given year.

References

Aagaard, K., L.K. Coachman, and E. Carmack (1985): On the halocline of the

Arctic Ocean. J. Geophys. Res., 90, 4833–4846.

Cavalieri, D.J., and S. Martin (1994): The contribution of Alaskan, Siberian, and

Canadian coastal polynyas to the cold halocline layer of the Arctic Ocean. J.

Geophys. Res., 99, 18,343–18,362.

Coachman L.K. (1986): Circulation, water masses, and fluxes on the southeastern

Bering Sea shelf. Cont. Shelf. Res., 5, 23–108.

Hendricks, P.J., R.D. Muench, and G.R. Stegen (1985): A heat balance for the

Bering Sea ice edge. J. Phys. Oceanogr., 15, 1747–1758.

Muench, R.D., and J.D. Schumacher (1985): On the Bering Sea ice edge front. J.

Geophys. Res., 90, 3185–3197.

Niebauer, H.J. (1988): Effects of El Ni ̃no-Southern Oscillation and North Pacific
138 S.A. Macklin (ed.)

weather patterns on interannual variability in the subarctic Bering Sea. J.

Geophys. Res., 93, 5051–5068.

Niebauer, H. J., V.A. Alexander, and S. Hendricks (1990): Physical and biological

oceanographic interaction in the Spring Bloom at the Bering Sea marginal ice

edge zone. J. Geophys. Res., 95, 22,229–22,242.

Niebauer H.J., V. Alexander, and S.M. Henrichs (1995): A time-series study of the

spring bloom at the Bering Sea ice edge, I, Physical processes, chlorophyll and

nutrient chemistry. Cont. Shelf Res., 15, 1859–1878.

Ohtani, K., and T. Azumaya (1995): Interannual change of the sea conditions on

the continental shelf and its influence on abundance of walleye pollock in the

eastern Bering Sea. Can. J. Fish. Aquat. Sci., Special Pub., 121, 87–95.

Overland, J.E., and C.H. Pease (1982): Cyclone climatology of the Bering Sea and

its relation to sea ice extent. Mon. Weather Rev., 110, 5–13.

Pease, C.H. (1980): Eastern Bering Sea ice processes. Mon. Weather Rev., 108,

2015–2023.

Roach, A.T., K. Aagaard, C.H. Pease, S.A. Salo, T. Weingartner, V. Pavlov, and

M. Kulakov (1995): Direct measurements of transport and water properties

through Bering Strait. J. Geophys. Res., 100, 18,443–18,457.

Schumacher, J.D., K. Aagaard, C.H. Pease, and R.B. Tripp (1983): Effects of a shelf

polynya on flow and water properties in the northern Bering Sea. J. Geophys.

Res., 88, 2723–2732.

Stabeno, P.J., J.D. Schumacher, R.F. Davis, and J.M. Napp (1998): Under-ice

observations of water column temperature, salinity and spring phytoplankton

dynamics: Eastern Bering Sea shelf. J. Mar. Res., 56, 239–255.

Wyllie-Echeverria, T. (1995a): Sea-ice conditions and the distribution of walleye

pollock and the Bering and Chukchi Sea shelf. In Climate Change and Northern

Fish Populations, R.J. Beamish (ed.), Can. Spec. Publ. Fish. Aquat. Sci., 121,

87–95.

Wyllie-Echeverria, T. (1995b): Seasonal sea ice, the cold pool and gadid distribution

on the Bering Sea shelf. Ph.D. Thesis, University of Alaska, Fairbanks, 281 pp.
Bering Sea FOCI Final Report 139

Part 4

Administration and management of the Bering Sea

FOCI Program (S. Allen Macklin)

4.1 Beginning of the Project

Bering Sea Fisheries-Oceanography Coordinated Investigations (BS FOCI)

developed from the need to better understand environmental characteristics

and processes affecting the rapidly developing walleye pollock fishing industry in the Bering Sea. NOAA previously had funded a study in the Gulf of

Alaska, Shelikof Strait FOCI (Kendall et al., 1996), that had established an

understanding of processes affecting survival of young pollock. Although the

Shelikof Strait pollock fishery was of commercial importance, it was dwarfed

by the catch of pollock in the Bering Sea.

A chronology of BS FOCI is provided in Table 4.1. In May of 1990 BS

FOCI published an implementation plan (BS FOCI, 1990) for a FisheriesOceanography Coordinated Investigation of Pollock in the Bering Sea. This

plan was in response to the establishment of a coastal fisheries ecosystems (CFE) project by NOAA’s Coastal Ocean Program (COP; Boyles and

Scavia, 1993; Wenzel and Scavia, 1993). The goal of CFE was to reduce

uncertainty in resource management decisions through ecological research.

The premise of BS FOCI was that the Bering Sea was among the most

productive of northern high-latitude seas. The primary commercial resource

was walleye pollock, prevalent on the continental shelves of the Bering Sea

and in the basin. With the passage of the Magnuson Fisheries Conservation

and Management Act of 1976, the coastal fishery came under management

control of the United States. By the 1980s, a domestic fishery industry

developed to replace foreign industry in the U.S. Exclusive Economic Zone

(EEZ). However, over-exploitation in the international deep basin was an

important issue in the management of the fishery, as basin pollock stocks

were thought to be linked to stocks in the EEZ. Despite biological assessment

of the southeast Bering Sea shelf through a number of research programs

provided by the National Science Foundation and NOAA with the Bureau

of Land Management, the information base for the region, especially the

deep basin and its ties to the shelf, was almost nonexistent.

BS FOCI’s implementation plan called for examination of the hypothesis

that transport of larval pollock from the deep Aleutian basin to the continental shelf contributes to the viability of U.S. fisheries. Four objectives

were established, based on research recommendations from an International

Scientific Symposium on Bering Sea Fisheries held in Sitka, Alaska during

July 1988 (Aron and Balsiger, 1989):

1. Determine the differences between pollock spawning aggregations

through techniques of molecular biology.

2. Determine circulation of the Bering Sea, including the deep basin and

the extensive eastern continental shelf.
140 S.A. Macklin (ed.)

Table 4.1: A chronology of significant Bering Sea FOCI events.

Year Month Event

1990 June Implementation Plan with hypothesis that transport of larval pollock from the deep Aleutian Basin to the southeastern shelf contributes to the viability of U.S. fisheries

1991 March Project Study Plan 1991–1996

August Cruise: large scale CTD and ADCP survey of the Bering Sea basin

November Principal investigators organizational meeting, Seattle, Washington

1992 April Cruise: first deployment of Peggy Bering Sea, larval survey

September Cruise: recover Peggy Bering Sea

1993 March Cruise: deploy Peggy Bering Sea

April Cruise: larval survey

August Principal investigators meeting in Portland, Oregon

September Cruise: recover Peggy Bering Sea, CTD survey

October Sponsored Juvenile Pollock Symposium, Seattle, Washington

November Reviewed by National Research Council, Washington, D.C.

1994 January Reviewed by National Research Council with Technical Advisors present, Seattle, Washington

February Cruise: deploy Peggy Bering Sea

April Cruise: larval survey

September Cruises: CTD survey, acoustics; Pribilof juvenile pollock studies, mooring recoveries

November Principal investigators meeting, Seattle, Washington

1995 March Cruise: deploy moorings

April Cruise: larval studies

May Cruise: larval studies

August– Cruises: moorings, Pribilof juvenile pollock studies

September

1996 February Cruise: deploy moorings

1996 April Cruise: moorings, CTD and larval survey

May Joint cruise and aircraft flights: moorings, groundtruth, primary productivity survey

September Cruises: Pribilof juvenile pollock studies; mooring recoveries

October Juvenile studies principal investigators synthesis meeting, Seattle, Washington

December Biophysical interactions principal investigators synthesis meeting, Seattle, Washington

1997 January Biophysical interactions principal investigators synthesis meeting, Seattle, Washington

March Juvenile studies principal investigators synthesis meeting, San Diego, California

June Publication of Bering Sea and North Pacific Ocean Theme Page on the Worldwide Web

September Larval ecology principal investigators synthesis meeting, Juneau, AK

3. Determine patterns and processes involved in vertically mixing the

water column.

4. Study how different oceanographic domains in the Bering Sea contribute to larval growth and mortality.

After the implementation plan was reviewed by the CFE Advisory Committee in January 1991, BS FOCI was asked to submit a Project Study Plan

(BS FOCI, 1991) to describe research from 1991 through 1996. The Project

Study Plan, submitted in March 1991, identified two goals for the project.

The first goal was to address the issues of pollock stocks in the Bering Sea

based on objectives 1 and 2. The second goal dealt with the processes that

affected the survival of basin pollock in their earliest life stages and their

subsequent recruitment, and was based on objectives 3 and 4. During the

last 2 years of BS FOCI, the arena for recruitment studies was shifted to the
Bering Sea FOCI Final Report 141

Table 4.2: Bering Sea FOCI Executive Committee

William Aron (ex officio) Allen Macklin (coordinator)

NOAA/Alaska Fisheries Science Center NOAA/Pacific Marine Environmental Laboratory

Eddie Bernard (ex officio) Jeffrey M. Napp

NOAA/Pacific Marine Environmental Laboratory NOAA/Alaska Fisheries Science Center

Stephen Bollens James E. Overland

San Francisco State University NOAA/Pacific Marine Environmental Laboratory

Lewis Haldorson James D. Schumacher

University of Alaska Fairbanks NOAA/Pacific Marine Environmental Laboratory

Arthur Kendall Jr. Gary L. Stauffer

NOAA/Alaska Fisheries Science Center NOAA/Alaska Fisheries Science Center

southeastern shelf. A component examining juvenile pollock near the Pribilof Islands during the late summer and fall of their birth year was added

in 1994.

4.2 Project Management

The Project Study Plan designated co-project managers from the Alaska

Fisheries Science Center (AFSC; G. Stauffer) and the Pacific Marine Environmental Laboratory (PMEL; J. Overland). The co-managers, together

with senior scientists from each laboratory and the laboratory directors,

formed an Executive Committee (Table 4.2). This committee was responsible for directing BS FOCI consistent with COP’s guidelines, coordination

of BS FOCI with other NOAA base programs concerned with Bering Sea

pollock, and evaluation of proposals from academic institutions. A project

coordinator was added to the Executive Committee in August 1993, and two

academic members were added in 1994 in response to a suggestion by the

National Research Council (1994).

The plan further identified an intramural research team of scientists from

the Alaska Fisheries Science Center and the Pacific Marine Environmental

Laboratory. These scientists brought expertise on Bering Sea pollock stocks,

circulation, and recruitment processes, including the collected wealth of Shelikof Strait FOCI established in 1985. To provide balance and expertise in

needed areas, extramural contracts were established in September 1991 for

genetic studies, satellite remote sensing of circulation, and studies on vertical distribution of zooplankton. A Principal Investigator group consisted

of the two project managers and all the principal participating scientists.

This group met at least quarterly, published a quasi-annual Progress and

Plans document, coordinated all contracts with academic research institutions, and obtained peer review of scientific results at national meetings and

in refereed journal publications.

At the end of the first year, COP conducted a review of the project. As a
142 S.A. Macklin (ed.)

Table 4.3: Bering Sea FOCI Technical Advisory Committee

Dr. Michael Dagg Dr. Thomas Royer

Louisiana University Marine Consortium Old Dominion University

Chauvin, LA 70344 Norfolk, VA 23505

Mr. Bart Eaton Dr. Al Tyler

Trident Seafoods Corporation University of Alaska Fairbanks

Seattle, WA 98107 Fairbanks, AK 99775-1080

Dr. Eileen Hofmann Dr. Warren Wooster

Old Dominion University University of Washington

Norfolk, VA 23505 Seattle, WA 98195-5685

Dr. William Leggett

Queens University

Kingston, Ontario

Canada K7L 3N6

result of this review, BS FOCI implemented a Technical Advisory Committee

(Table 4.3) to help guide the project.

4.3 Budget

Funds for BS FOCI were allocated in the first year at just under a million

dollars. The project was level funded through 1995, then funds tapered off

during the final 2 years. The funding profile for BS FOCI was

FY 1991 $950K

FY 1992 $950K

FY 1993 $950K

FY 1994 $950K

FY 1995 $950K

FY 1996 $750K

FY 1997 $200K

4.4 Competitive Process and Research Cycles

For the first round of research (FY 1991 through FY 1993), AFSC and

PMEL FOCI scientists submitted work statements addressing the objectives

of Phase I and Phase II research. These were evaluated by the co-managers

and a team of intramural scientists was established. To provide academic balance, proposals were solicited from the outside community in a competitive

process for $260K. These were evaluated by the co-managers and Executive

Committee. From the evaluations, extramural contracts were established in

September 1991 for genetic studies, satellite remote sensing of circulation,

and studies on vertical distribution of zooplankton to last through FY 1993.

In FY 1993, proposals for FY 1994 and FY 1995 research were solicited

from the scientific community at large. Proposals were evaluated by the

Executive Committee and the Technical Advisory Committee. Finally, the

Executive Committee solicited work statements from specific researchers for
Bering Sea FOCI Final Report 143

FY 1996 to complete objectives of the project. Funds in FY 1997 were used

to support publications, analysis of samples and data, synthesis meetings,

and development of data access through the World Wide Web. Table 4.4

lists all BS FOCI research components.

BS FOCI developed collaborations with Russian, Korean, and Japanese

scientists. These associations provided scientific leverage through the sharing

of data and research vessels.

4.5 Meetings and Workshops

BS FOCI intramural researchers met monthly at a FOCI Principal Investigators meeting. An electronic bulletin board was established to share notice

and agenda of these meetings, and to publish their minutes, so that extramural researches could be represented and informed.

The Executive Committee met several times a year to establish procedure, evaluate proposals, and provide guidance.

During October 1993, BS FOCI hosted a 3-day international workshop

in conjunction with the second annual meeting of the North Pacific Marine

Science Organization. The subject of the workshop was the importance of

prerecruit walleye pollock to the Bering Sea and North Pacific ecosystems

(Brodeur et al., 1996).

The full suite of principal investigators met on several occasions to discuss

research plans and progress and to implement field plans.

Small working groups of principal investigators associated with juvenile

pollock ecology and biophysical processes held synthesis meetings in the fall

and winter of 1996–1997.

4.6 Field Experiments

BS FOCI conducted more than 20 cruises and one aircraft expedition during

its 7-year lifetime. Because the project was focused on the early life history

of pollock and determining circulation and stock structure of pollock, the

field season developed a recurring routine. In general, the earliest cruises of

the year were conducted during February and March. Their purpose was to

deploy moorings for the late winter, spring, summer, and early fall observation period, to ascertain ground truth for the moorings, and to sample water

conditions prior to spawning of pollock in the spring. During spring, cruises

worked to sample larval pollock distributions as well as their prey and predators, to monitor the progress of the nutrient-phytoplankton-zooplankton cycle, and to document biophysical processes important to survival of larval

pollock. Fall cruises observed the ecosystem associated with juvenile pollock

in the Pribilof Islands habitat and recovered moorings.

The project utilized a number of research vessels. The primary carrier

was the NOAA Ship Miller Freeman. Other vessels supporting BS FOCI

were the NOAA Ship Surveyor and the Japanese Fishery Research Vessel

Oshoro Maru.
144 S.A. Macklin (ed.)

Table 4.4: Bering Sea FOCI research components and principal

investigators.

Component Principal Investigator

Larval feeding mechanisms of walleye pollock Kevin M. Bailey

NOAA/Alaska Fisheries Science Center

U.S./Japan cooperative studies Kevin M. Bailey

NOAA/Alaska Fisheries Science Center

Population ecology of walleye pollock Kevin M. Bailey

NOAA/Alaska Fisheries Science Center

Dennis A. Powers

Stanford University

Modeling the upper ocean production dynamics of

plankton and larval pollock in the Bering Sea

Stephen Bollens

San Francisco State University

Spatial and temporal characteristics of wind forcing of

the Bering Sea

Nicholas A. Bond

JISAO/University of Washington

Impact of invertebrate predators on walleye pollock

larvae

Richard D. Brodeur

NOAA/Alaska Fisheries Science Center

Juvenile pollock studies Richard D. Brodeur

NOAA/Alaska Fisheries Science Center

Larval pollock nutritional condition assay Michael Canino

NOAA/Alaska Fisheries Science Center

Basin vertical processes: mixed-layer dynamics from

the Peggy Bering Sea mooring

Edward D. Cokelet

NOAA/Pacific Marine Environmental Laboratory

Determining chlorophyll concentration from ocean

color measurement in the Bering Sea

John Cullen and Richard Davis

Dalhousie University

Bimodal distribution of juvenile pollock in the southeastern Bering SeaMiriam Doyle

JISAO/University of Washington

Growth, transport, and mortality studies of larval

walleye pollock

Robert C. Francis

University of Washington

Feeding ecology of larval walleye pollock in oceanic and

neritic domains of the Bering Sea: effects of variation

in prey

Lewis J. Haldorson

University of Alaska Fairbanks

An aggregated ecosystems model for the southeastern

Bering Sea

Albert J. Hermann

JISAO/University of Washington

Ichthyoplankton collections in the eastern Bering Sea Arthur W. Kendall, Jr.

NOAA/Alaska Fisheries Science Center

A retrospective analysis of GEOSAT altimeter data in

the Bering Sea

Robert Leben

University of Colorado

Role of protozoa in the diet of larval pollock in the

Bering Sea

Evelyn J. Lessard

University of Washington
Bering Sea FOCI Final Report 145

Table 4.4: (continued).

Component Principal Investigator

Monitoring of mesoscale ocean processes by synthetic

aperture radar (SAR)

Antony K. Liu

NASA/Goddard

Food chain dynamics: spring bloom hypothesis and

larval survival

Jeffrey M. Napp

NOAA/Alaska Fisheries Science Center

Otolith technique for tracing geographic life history of

pollock

Brenda L. Norcross

University of Alaska Fairbanks

Modeling Bering Sea circulation James E. Overland

NOAA/Pacific Marine Environmental Laboratory

Microcrustacean production potential during the onset

of feeding by walleye pollock larvae in the Aleutian

Basin and Bering Sea shelf

A.J. Paul

University of Alaska Fairbanks

The use of molecular techniques to dissect the genetic

architecture of pollock populations: analysis of mitochondrial and nuclear genes by the polymerase chain

reaction

Dennis A. Powers

Stanford University

Circulation of the eastern Bering Sea: Aleutian North

Slope Flow

Ronald K. Reed and Phyllis J. Stabeno

NOAA/Pacific Marine Environmental Laboratory

Larval transport and mesoscale circulation James D. Schumacher

NOAA/Pacific Marine Environmental Laboratory

Shelf-slope exchange along the eastern Bering Sea shelf

break

James D. Schumacher and Phyllis J. Stabeno

NOAA/Pacific Marine Environmental Laboratory

Data integration system and theme page for the Bering

Sea

Nancy Soreide

NOAA/Pacific Marine Environmental Laboratory

Nutritional condition of larval walleye pollock Gail H. Theilacker

NOAA/Alaska Fisheries Science Center

Relationships between pollock distribution and extent

of seasonal sea ice on the Bering Sea shelf

Tina Wyllie-Echeverria

JISAO/University of Washington

Phytoplankton dynamics from moored optical instruments in the southeastern Bering SeaJ. Ronald V. Zaneveld

Oregon State University
146 S.A. Macklin (ed.)

4.7 Data Dissemination

In order to facilitate data exchange between investigators and to make BS

FOCI data available to the scientific community, the project underwrote

creation of the Bering Sea and North Pacific Ocean Theme Page, a World

Wide Web resource at http://www.pmel.noaa.gov/bering. The theme

page provides pathways to much of the physical and biological data collected

by BS FOCI, as well as other information grouped by scientific discipline.

The Bering Sea Ecosystem Biophysical Metadatabase, an annotated index

of data holdings, is available through the theme page.

4.8 Project Reviews

BS FOCI was reviewed formally on two occasions. The first was an internal

review by COP in the spring of FY 1992. As a result of this review, the

project convened its Technical Advisory Committee.

A more extensive review was conducted by the National Research Council

(1994) during FY 1994. There were two phases of this review of accomplishments and plans of the NOAA Coastal Ocean Program. The first phase was

a briefing of the panel by senior project scientists in Washington D.C. The

second was held in Seattle with BS FOCI’s technical advisors present. At

this meeting, project principal investigators gave a series of presentations to

the panel. Administrative changes suggested by the panel and adopted by

BS FOCI were the expansion of the Executive Committee to include academic investigators, formalization of the competitive process, and formation

of small working groups based on the scientific structure of the project.

The importance of the Bering Sea’s commercial resources and the success of BS FOCI in addressing questions pertaining to walleye pollock in the

Bering Sea have helped generate increased interest in the Bering Sea ecosystem. New programs such as COP’s Southeast Bering Sea Carrying Capacity

and NOAA’s Arctic Research Initiative, as well as ongoing research by FOCI,

build on these concepts developed by BS FOCI, and continue to advance our

understanding of the complex, productive ecosystem of the Bering Sea.

4.9 References

Aron, W., and J. Balsiger (1989): Proceedings of the International Scientific Symposium on Bering Sea Fisheries. NOAA Tech. Memo. NMFS F/NBC-163, 424 pp.

(available from Alaska Fisheries Science Center, 7600 Sand Point Way N.E.,

Seattle, WA 98115-0070).

Boyles, R., Jr., and D. Scavia (1993): Innovative coastal ocean science at NOAA.

Sea. Tech., 34, 10–16.

Brodeur, R.D., P.A. Livingston, T.R. Loughlin, and A.B. Hollowed (eds.) (1996):

Ecology of juvenile walleye pollock, Theragra chalcogramma. U.S. Department

of Commerce, NOAA Technical Report NMFS 126, 227 pp. (available from

Alaska Fisheries Science Center, 7600 Sand Point Way N.E., Seattle, WA 98115-

0070).

BS FOCI (1990): Bering Sea FOCI Implementation Plan FY 1991–1996. U.S.

Department of Commerce, National Oceanic and Atmospheric Administration,

16 pp. (available from Pacific Marine Environmental Laboratory, 7600 Sand

Point Way N.E., Seattle, WA 98115-0070).
Bering Sea FOCI Final Report 147

BS FOCI (1991): Bering Sea FOCI Project Study Plan FY 1991–1996. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, 28pp.

(available from Pacific Marine Environmental Laboratory, 7600 Sand Point Way

N.E., Seattle, WA 98115-0070).

Kendall, A.W., Jr., R.I. Perry, and S. Kim (1996): Fisheries oceanography of walleye

pollock in Shelikof Strait, Alaska. Fish. Oceanogr., 5(Suppl. 1), 203 pp.

National Research Council (1994): A Review of the Accomplishments and Plans

of the NOAA Coastal Ocean Program. National Academy Press, Washington,

D.C., 115 pp.

Wenzel, L., and D. Scavia (1993): NOAA’s Coastal Ocean Program. Oceanus, 36,

85–92.
148 S.A. Macklin (ed.)
Bering Sea FOCI Final Report 149

Part 5

Selected monitoring, modeling, and technical

achievements (compiled by S. Allen Macklin)

The development and application of new technology allows the field of fisheries oceanography to move forward. During BS FOCI’s 61⁄2-year lifetime,

its scientists and technicians made numerous and significant technological

contributions to the field. Some of these achievements were specific to the

Bering Sea region, some were specific to walleye pollock, and some were

more wide-ranging in their applications. In the following sections, selected

achievements are discussed under the headings of monitoring, modeling, and

technology.

5.1 Monitoring

BS FOCI used moorings, satellite-tracked drifters, and shipboard measurements to monitor physical and biological oceanographic conditions in the

several distinct domains of the Bering Sea basin and the eastern Bering Sea.

a. refined understanding of circulation in the Bering Sea basin through

observations with vessel-mounted acoustic Doppler current profiler

(Cokelet et al., 1996) and satellite-tracked drifters (Stabeno and Reed,

1994):

A month-long circumnavigation of the Bering Sea basin in August 1991

was one of BS FOCI’s first field operations. During the cruise, scientists

made the first use of an acoustic Doppler current profiler in the Alaskan

Stream and Bering Sea. Observations of three-dimensional current velocity led to an increased knowledge of circulation and transport in

the Bering Sea basin and improved the ability to compute geostrophic

circulation from hydrographic casts.

From 1986 through 1996 (and continuing since then under sponsorship from other research funding), BS FOCI deployed more than 120

satellite-tracked drifters in the North Pacific Ocean and Bering Sea.

Most drift buoys were drogued at 40 m. A composite current pattern was derived from data telemetered by these drifters. This pattern

helped identify large- and mesoscale features of circulation and led to

discovery of a new current, the Aleutian North Slope Current (Reed

and Stabeno, 1998).

b. unique time series of water column temperature, salinity, estimated

chlorophyll-a, and phytoplankton fluorescence during ice advance and

retreat (Stabeno et al., 1998):

During 1995 three surface moorings were deployed over the southeast

Bering Sea shelf. Each mooring had instruments that measured temperature, salinity and fluorescence. After the moorings were deployed
150 S.A. Macklin (ed.)

in February, the most severe ice conditions in the last 20 years developed. Two of the moored platforms were struck by the sea ice but

continued to function. They provided unique time series of watercolumn temperature, salinity, chlorophyll-a and fluorescence under an

advancing and retreating ice field. One platform was located in the

weakly advective middle shelf regime. Here, contrary to earlier findings, chlorophyll-a concentrations increased prior to the formation of

a well-defined two-layer system. Events of strong advection, rather

than vertical fluxes, dominated changes in water column structure and

properties. These advective events provide a mechanism for nutrients

(required to support the rich blooms that occur over the middle shelf

during spring) to be transported onto the middle shelf. A second mooring was located in the more advective outer shelf. The ice also reached

this site, and chlorophyll-a concentrations increased with the advent

of ice. The final mooring was deployed to the east of Unimak Pass.

Sea ice was not advected this far south, and the spring bloom did not

occur until May.

c. upper ocean phytoplankton survey (Davis et al., 1997a):

For its last field experiment, in spring 1996, BS FOCI conducted a

survey of sea surface chlorophyll over the southeastern Bering Sea using a research aircraft and ship. The project documented the spatial

and temporal evolution of chlorophyll concentration during the spring

bloom in the Bering Sea and how this concentration related to the

ocean’s physical characteristics. Chlorophyll concentration was estimated from the aircraft using remote color-sensing instrumentation

designed to detect upwelling radiance from the ocean. The ocean’s

physical characteristics were assessed using air-expendable bathythermographs deployed from the plane; instrumented, moored buoys; and

by CTD casts and ADCP transects aboard ship. Preliminary results

showed higher chlorophyll concentrations in the northern portion of

the domain where sea ice was melting, and a prominent 100 × 200 km

patch southeast of the Pribilof Islands with concentrations an order of

magnitude greater than background levels. This patch was in a region

of the shelf where pollock spawning occurs.

5.2 Modeling

BS FOCI used models to conceptualize program strategies, to expand the

time-space domain of field observations, to guide program direction through

hypothesis generation, and to understand features of biophysical processes.

a. numerical model of circulation of the Bering Sea basin and exchange

with the North Pacific Ocean (Overland et al., 1994):

At the beginning of the Bering Sea FOCI project, use was made of

a high-resolution, 1/8◦-grid, numerical model to investigate the circulation of the Bering Sea basin and the adjacent North Pacific Ocean.
Bering Sea FOCI Final Report 151

The modeling was based on the Navy Layered Ocean Model, one of

the highest-resolution ocean circulation models at the time, and run

on the University of Alaska Fairbanks’ supercomputer. There was a

generally cyclonic, but spatially complex and non-stationary, circulation within the Bering basin, fed by flow through the Aleutian passes.

The numerical study demonstrated that internal flow instabilities, and

not just external forcing such as wind and inflow current, contribute

to substantial interannual variability in the circulation of the Bering

Sea and adjacent northwestern Pacific Ocean.

b. coupled, one-dimensional, biophysical model investigating production

dynamics of the pelagic ecosystem with respect to growth of larval

pollock (Francis et al., 1998; Bollens et al., in preparation):

A coupled, one-dimensional, biophysical model investigated production dynamics of the pelagic ecosystem with respect to growth of larval pollock. The approach used field observations to determine rates

and appropriate species composition for several of the distinct physical

and biological domains in the eastern Bering Sea. The model included

stage-structured dynamics of copepod populations (Calanus and Neocalanus) and larval pollock feeding and growth. The temporal behavior

of the mixed layer was obtained from observations from Peggy Bering

Sea, a moored biophysical platform. Model results showed that the

species composition of zooplankton has a strong influence on growth

of larval pollock, and the presence of protozoan prey becomes important when young copepods are scarce, i.e., during early spring over the

slope. Results from the model also suggested that variability of the

mixed-layer depth has significant impact on larval growth by affecting

lower trophic level production. These results led to the addition of a

field research component that developed a new method for live-staining

protists and showed that microprotozoan biomass levels are sufficient

to augment prey levels and support estimated metabolic needs of firstfeeding larval pollock.

5.3 Technology

At the beginning of the project, there was scant knowledge of processes that

affect recruitment of walleye pollock in the Bering Sea. Some findings from

FOCI’s Shelikof Strait project were applicable, but steps had to be taken to

develop new methods to address specifics of the Bering Sea environment and

ecosystem. BS FOCI made nearly 20 significant technological developments

that furthered understanding of general and regional physical and biological

oceanography.

a. a modified PROTEUS mooring that withstands the arctic marine climate of the Bering Sea and measures winds, insolation, air temperature, humidity, salinity, and temperature at ten depths, currents from

acoustic Doppler current profiler and acoustic current meters, acoustic

backscatter, and chlorophyll absorption (Cokelet and Stabeno, 1997):
152 S.A. Macklin (ed.)

Because there were no continuous time series of biophysical conditions

from pre-spring bloom conditions through the summer, BS FOCI developed and deployed a surface mooring, Peggy Bering Sea, in the southeast basin at 2195 m depth in the spring and summer of 1992–1994

and the winter of 1994. It recorded the first long-term oceanographic

time series in the basin. The winter observations are particularly valuable due to the lack of wintertime measurements in this region. The

platform was a PROTEUS (PROfile TElemetry of Upper ocean currentS) similar to moorings deployed in the tropical Pacific Ocean, but

modified to withstand the arctic marine climate of the Bering Sea.

Included in its suite of measurements were winds, insolation, air temperature, humidity, salinity, and temperature at ten depths, currents

from acoustic Doppler current profiler and acoustic current meters,

acoustic backscatter, and chlorophyll absorption. Some of the observations were telemetered real time via satellite and System ARGOS.

Useful information for understanding the Bering Sea ecosystem was deduced from Peggy Bering Sea measurements. At that part of the basin

there is a weak background flow of a few cm s−1 and little density

variation with internal tides superimposed. Anticyclonic (clockwise)

eddies pass by sporadically, inducing currents up to ∼8 0 cm s−1 and

depressing isopycnals by as much as ∼200 m. The thermal structure

in the upper 400 m shows a deep temperature maximum from warm

Alaskan Stream inflows and a minimum above due to winter cooling.

A sea surface cooling event was observed in the late winter of 1994,

with cold water penetrating to ∼120 m depth. Spring warming begins

in late April to early May of each year, marked by the arrival of the

3.75◦C isotherm. The local wind plays little role in forcing ocean currents at the site except at the inertial frequency. Because some data

were telemetered in real time, Peggy Bering Sea permitted direction of

field sampling to provide in situ measurements by ship. The mooring

design later was modified for shallow-water use, and two moorings were

deployed during early March 1995—one over the outer and one over

the middle southeastern Bering Sea shelf. They were inundated by sea

ice, providing unique time series of water column temperature, salinity, estimated chlorophyll-a, and phytoplankton fluorescence during ice

advance and retreat.

b. remote methods for determining mesoscale ocean circulation and features using high resolution synthetic aperture radar (Liu et al., 1994)

and radar altimetry (Stabeno et al., in preparation) from satellites,

and shipboard acoustics (Brodeur et al., 1996):

Results from the slope waters of the eastern Bering Sea indicated that

the highest abundances of pollock larvae often reside in eddies. To

examine the nature of biophysical processes present in these features

and determine their influence upon survival required in situ observations. Finding a reliable method to locate an eddy for field studies
Bering Sea FOCI Final Report 153

was a challenge. Although infrared imagery has proved useful, cloud

cover and generally weak sea surface temperature gradients limit this

approach for the Bering Sea. High-resolution synthetic aperture radar

(SAR) eliminates both of these constraints. Mesoscale features are imaged by SAR through several possible mechanisms that are not well

understood, including current-induced wave refraction. SAR images

were examined for mesoscale features in Alaskan coastal waters, and

BS FOCI maintained an image library. A new method for time-varying

signal analysis, called the Wavelet Transform was developed (Liu et al.,

1997) and gives spectral decompositions via the scale concept. A twodimensional wavelet transform is a highly efficient band-pass-filter that

can be used to separate various scale processes and show their relative

phase and location as a matched filter detector. A two-dimensional

Gaussian wavelet transform of a SAR image can be used with threshold

as an edge detector for small-scale features. The evolution of mesoscale

features such as oil slicks, fronts, eddies, and internal waves can be

tracked by wavelet analysis using satellite data from repeating paths.

Real-time, remote tracking of eddies enabled BS FOCI to guide sampling by a Japanese research vessel working cooperatively with project

scientists during summer 1993.

A new technology, near real-time altimetry, was employed in the Bering

Sea to help locate an anticyclonic eddy for field surveys. Near realtime data from TOPEX/POSEIDON (T/P) and ERS-2 were processed

at the University of Colorado’s Center for Astrodynamics Research

(CCAR) to map sea surface height anomalies in the southeast Bering

Sea basin, and these maps were posted daily on the CCAR website

(http://www-ccar.colorado.edu/∼leben/bering/). This method

came to fruition for Bering Sea research in the year following BS

FOCI’s final field operations. In May 1997, the development of an

8-cm high at 55◦N, 169◦W was monitored by a BS FOCI scientist

using maps posted on the CCAR website. Using the near real-time information supplied by the satellite altimetry, she was able to direct the

NOAA ship Miller Freeman to the location of the eddy. Subsequent

surveys and satellite tracked drifters confirmed eddy circulation.

Acoustic backscatter signals from hull-mounted echo sounders also

were used to identify and characterize mesoscale biophysical features

in the ocean. Higher frequency transponders are able to scatter their

acoustic energy from zooplankton and other smaller marine life that

are contained by eddy circulation.

c. method for measuring the growth and retreat of seasonal sea ice along

a longitudinal meridian (Wyllie-Echeverria, 1996):

Data for the position of the ice edge along 169◦W longitude were extracted from products of the Navy/NOAA Joint Ice Center’s data base

presenting weekly concentration and position of sea ice cover. This lon-
154 S.A. Macklin (ed.)

gitude was chosen because it lies over open water for the entire extent

of the Bering and Chukchi shelves and intersects the shelf break at

the shelf’s southernmost reaches. Data were verified using weekly ice

charts for the western Arctic provided by the Naval Polar Oceanography Center. Comparison with areal ice coverage between 160◦W and

180◦W (Chapman and Walsh, 1993) revealed that the southernmost

latitude reached by ice along 169◦W is significantly correlated with icecovered shelf area (r = 0.91). This method developed by BS FOCI for

measuring the growth and retreat of seasonal sea ice along a longitudinal meridian was also adopted for application by NMFS to evaluate

sea ice conditions in the western Bering Sea.

d. development of digitally recording chlorophyll absorption meters and

an anti-fouling system to enable their long-term deployment (Davis et

al., 1997b):

BS FOCI has played an instrumental role in the ongoing development

and deployment of digitally recording chlorophyll absorption meters.

These instruments enable accurate, long-term, in situ monitoring of

phytoplankton standing stock, and are unique in the world. Absorption data from the meters are used to calculate accurate estimates of

chlorophyll concentration by the simple subtraction of a baseline value

for background absorption. Time series of phytoplankton biomass coupled with hydrographic properties can then be used to validate biophysical algal growth models and investigate ecological processes on

several time scales. BS FOCI was one of the first programs to make

use of these meters. Peggy Bering Sea served as a test platform for

this developing technology. The development of a simple, low-cost,

low-toxicity antifoulant system has made it possible to collect longterm, high-quality data on in situ light absorption, even in remote

environments such as the Bering Sea. The ability to deploy optical

instruments for extended periods of time produces considerable savings in resources since periodic servicing of instruments may be made

at longer intervals. First-generation optical instrumentation for the

detection of spectral absorption and attenuation of light was included

as part of the 1993 Peggy Bering Sea mooring. For this deployment, a

chemical method was developed to reduce the extent of the biofouling.

To prevent biofouling in the sample chamber of the absorption meters,

a novel system was implemented that utilized the enclosed flow tube

of the instruments. A perforated inner canister was filled with solid

bromine tablets and then placed into a vented outer canister. The

holes in the inner canister allow the slow dissolution of the bromine

tablets into the sea water within the outer canister, with the rate of

bromine dissolution being determined by the size of the holes. A dissolution was chosen such that a concentration of ∼30 parts per million

(ppm) built up in the enclosed flow tube of the optical instrument

within 15 min after a sampling period, a concentration about 10 times

the minimum toxic level determined from tests on natural waters from
Bering Sea FOCI Final Report 155

Newport, Oregon. The sample chamber was flushed for 5 s prior to

data collection using a Sea-Bird pump model 5T, which provided more

than three full volume exchanges in the flow tube. This flushing insured that the bromine did not compromise absorption measurements.

e. relationships between ADCP acoustic backscatter and zooplankton

abundance (Cokelet et al., in preparation):

The Peggy Bering Sea surface mooring contained, along with other

meteorological and oceanographic instruments, a downward-looking

153-KHz acoustic Doppler current profiler (ADCP) to measure vertical profiles of ocean currents. The ADCP computes ocean currents by

measuring the Doppler frequency shift of sound of a known transmitted frequency as it reflects off scatterers carried by the moving water.

The scatterers themselves are usually zooplankton whose concentration and time-dependent behavior are valuable for biological studies.

One BS FOCI research objective was to determine the zooplankton

biomass from ADCP measurements. To do so involved a two-step process: determining the volume backscattering strength (Sv in dB) from

ADCP-measured quantities and relating Sv to the zooplankton concentration.

The volume backscattering strength at a fixed acoustic frequency is

a physical property of the scattering medium and represents its ability

to reflect sound. It cannot be measured directly by the ADCP. As a

byproduct of the current measurements, the ADCP records automatic

gain control counts that can be related to Sv via factory-specified relationships utilizing the thermally induced circuit noise to which the

signal is referenced. This circuit noise was determined by tank-testing

the ADCPs. Tracking the noise calibrations over time gave an indication of calibration variability and has been used to determine the

overall error in the zooplankton biomass via a new error analysis.

To relate the volume backscattering strength to the zooplankton biomass, BS FOCI collected zooplankton from 23 MOCNESS (Multiple

Opening Closing Net Environmental Sampling System) hauls with up

to nine nets each, giving a total of 111 samples. Computer software

was developed to integrate the ADCP backscatter along the same timedepth trajectories as the net tows. Trajectory-averaged acoustic volume backscattering strength was then compared to zooplankton displacement volume which in turn was related to biomass via published

relationships. Not all of the MOCNESS tows were near the mooring, but all tows were made from a ship with an ADCP of the same

frequency as the mooring. Therefore, to provide the largest possible

sample size, Sv-zooplankton comparisons were also made for the shipboard ADCP whose noise level was calibrated at sea.

Results show that the logarithm of the zooplankton dry weight concen-
156 S.A. Macklin (ed.)

tration (DW mg m−3) is linearly related to the volume backscattering

strength (r2 = 0.61). The error analysis shows that the inferred biomass is correct to within a factor of two. The variance is probably

due to the size, orientation, and relative species composition of the

scatterers which were dominated by copepods (Neocalanus spp., Eucalanus bungii and Metridia pacifica). Observations give zooplankton

dry weight concentrations varying from vanishingly small at 300 m

depth to 400 mg m−3 at 14 m during the spring bloom. Rapid behavioral changes have been observed in which the zooplankton cease

their usual diel vertical migration from below 300 m to the surface

and concentrate in the upper 100 m during a phytoplankton bloom.

These quantitative, long-term time series of zooplankton biomass and

behavior are useful for understanding the Bering Sea ecosystem.

f. a dual-frequency hydroacoustic analytical procedure that pioneered visualization of distributions of upper-trophic-level predators and their

prey in marine ecosystems (Napp et al., submitted):

BS FOCI researchers collaborated with bio-acousticians from the Southwest Fisheries Science Center, La Jolla, California, to apply a dual

frequency hydroacoustic analytical procedure to examine distribution

patterns of predators (age-0 pollock) and prey (zooplankton) in structural fronts around the Pribilof Islands. The fronts are hypothesized to

be important habitat for age-0 pollock in the eastern Bering Sea. The

technique exploits the difference in volume backscattering measured at

two acoustic frequencies, 200 and 120 kHz. A 50-km transect from a

cruise during September 1994 near the Pribilof Islands was analyzed.

The differencing technique (Greenlaw, 1977; Mitson et al., 1996) assumes that only two different types and sizes of organisms dominate

the acoustic backscatter at these frequencies. Low differences indicate

that scattering is dominated by fish; high values are interpreted to be

primarily invertebrate zooplankton such as copepods and euphausiids,

the main prey of juvenile fish. During daytime conditions, the upper

layer to about 20 m is dominated by zooplankton. Juvenile fish are

distributed at mid depth and show a preference for the thermocline.

This could be a strategy for avoiding predators during daylight. At

night, there is a strong upward migration by fish over the inner front

and middle shelf, presumably to feed on the zooplankton in the upper

layer. After the fish migrate upwards, the bottom layer is dominated

by invertebrates. Juvenile pollock in the Gulf of Alaska have been

shown to be night feeders. This visualization of the diel pattern in

and around the structural front suggests how physics affects the distribution and behavior of fish and their prey through the tidal mixing

process. When coupled with net samples and physical measurements,

this dual-frequency technique has the potential to reveal important

information about the ecosystem.

g. a mitochondrial DNA probe to discern pollock population differences
Bering Sea FOCI Final Report 157

between the eastern and western Bering Sea (Bailey et al., 1998):

The genetics component of BS FOCI surveyed mitochondrial DNA

(mtDNA) sequence variation in pollock throughout a major portion of

its range. A total of 512 nucleotides were examined in 45 individuals

from populations representing the eastern and western portions of the

Bering Sea. Fourteen haplotypes were uncovered, of which three were

frequent enough to be of use in population differentiation. Testing of

an additional 119 samples allowed determination of significant differences among populations within the eastern and western portions of

the Bering Sea. A rapid restriction enzyme assay for mtDNA surveying

of a large number of pollock from all populations allows near real-time

analysis of genetic material from fish collected at sea, and also permits

retrospective analysis of samples that have been preserved in alcohol.

h. a microsatellite primer technique for pollock DNA that can discriminate sub-populations (Villa and Powers, in press):

In order to detect distinct pollock stocks within the Bering Sea, primers

were developed for the polymerase chain reaction that would amplify

microsatellite loci in pollock. Working from primers developed for Atlantic cod (Brooker et al., 1994), pollock-specific primers were developed for two microsatellites. Individual fish from six sites in the eastern

and western Bering Sea were screened. The microsatellite loci showed

a significant difference between eastern and western fish. Analysis of

additional samples collected northwest of the Pribilof Islands indicate

that there may also be a distinct stock structure between northern and

southern Bering Sea pollock.

i. methods for analyzing chemical deposition in pollock otoliths as a

record of the environment experienced by the larvae at various times

during their development (Severin et al., 1995):

The incorporation of dissolved oceanic constituents in the otoliths of

pollock has potential as a chemical tracer for reconstructing their early

life history. Wavelength dispersive spectrometers on an electron microscope were used to measure Na, Mg, P, S, Cl, K, Ca, and Sr concentrations on the outer margins of 57 juvenile walleye pollock otoliths

from five locations in the Gulf of Alaska and Bering Sea. Discriminant analyses that used various combinations of Na, P, K, Sr, and fish

standard length and/or age showed that 60–80% of the samples could

be assigned to the correct capture locality. While the concentrations

of some of the measured elements correlated with standard length of

age of the fish, there are measurable differences among localities when

concentrations are length of age corrected, mainly due to differences

in Na and K concentrations. Elemental composition of otoliths potentially could be used to assign fish from a mixed stock fishery to original
158 S.A. Macklin (ed.)

stocks, information that is greatly needed for the effective management

of fish stocks.

j. sophisticated 3D video cinematography to examine how larvae find

patches of prey and maintain themselves in these patches (Spring

1996):

Two synchronized CCD cameras were used with time-lapse video

recorders to film larvae under experimental laboratory conditions. A

shadowgraph filming technique was used with light provided by infrared diodes. Direct Linear Translation was used to retrieve 3D coordinates from the video images. The techniques developed were successfully applied to examine larval swimming speed, path aspect and

tortuosity in relation to the presence of food particles.

k. a new method for live-staining protists (Lessard et al., 1996):

A method was developed to live-stain protists with the fluorescent

nuclear stain, DAPI, for use in tracing ingestion of protists by larval

pollock. DAPI was shown to effectively live-stain eight species of protists and showed no toxic effects. The stain is simple to apply, easy

to visualize in larval guts using epifluorescence microscopy, and does

not appear to adversely affect the swimming behavior or growth rate

of protists. With this stain, it was shown that larval walleye pollock

are able to ingest a relatively small (60 μm) aloricate ciliate. This new

method provides a means for visually following the ingestion of previously undetectable, but potentially important, prey in larval pollock.

It provides a simple laboratory tool that can be used to determine

larval pollock gut evacuation rates and functional feeding responses to

different types and sizes of protists. Such laboratory measurements

would help to provide the information needed to predict the importance of heterotrophic protists in the diets of pollock larvae.

l. an antibody to protist-specific protein for an immunoassay to detect

ingestion by pollock larvae in the field (Howell-Kubler et al., 1996):

BS FOCI researchers used SDS-PAGE to survey the protein signatures of a large number of protists to identify a protein that would

be protist-specific for use in the development of an immunoassay for

ingestion of protists in pollock larvae. A 21-kD protein was found in

all heterotrophic protists, but not photosynthetic protists, copepods,

or pollock larvae. Antibodies to this protein have been developed and

purified, and are now available for immunoassay development. When

fully tested, the immunoassay will be used to detect the presence and

quantity of protist proteins in the guts of field-caught pollock larvae.

As protists generally do not leave visible remains after digestion, the

immunoassay method will provide a means for detecting otherwise undetectable food items in the guts of pollock larvae and allow the determination of the prevalence of protist ingestion in wild pollock larvae.
Bering Sea FOCI Final Report 159

m. a simple procedure for sampling and releasing a suspension of nuclei

from larval pollock muscle cells and for storage of the nuclei for subsequent analyses of larval condition (Theilacker et al., 1996):

Muscle cell nuclei were examined by marking them with fluorescent

dyes and submitting them to laser flow cytometry for cell cycle analysis. These methods were applied successfully to assess the nutritional

condition of pollock larvae in field studies.

n. techniques for determining larval pollock health by cytological examination of brain cells (Theilacker and Shen, 1993a, b):

This method includes marking RNA and DNA from a suspension of

brain cells with a fluorescent dye and quantifying the amounts of each

nucleic acid using laser flow cytometry.

o. techniques for distinguishing between Stage I and Stage II nauplii of

the copepods Metridia and Pseudocalanus (Siefert, 1998):

Food availability for pollock larvae is one of the key factors controlling larval growth and survival. To determine the role of the copepods

Metridia and Pseudocalanus in the ecosystem and to learn specifically

more about their role as prey of larval pollock, it is necessary to understand their life history and identify all their developmental stages.

Because the developmental stage of the prey changes with the ontogeny

of the fish, recent studies have stressed the importance of identifying

copepod nauplii of Metridia and Pseudocalanus to the lowest possible taxon. Past attempts to distinguish between the younger stages of

these dominant taxa have been unsuccessful. Recent work by BS FOCI

has enabled identification of the developmental stages of Metridia and

Pseudocalanus in field samples. Stage I nauplii of Metridia pacifica,

Stage I and II nauplii of Metridia lucens and the equivalent stages

of Pseudocalanus minus were reared from eggs to find morphological

characters for separating the genera at these stages. Differences in

naupliar body shape and caudal armature permit the differentiation

of Stage I and II Metridia from Pseudocalanus in southeastern Bering

Sea plankton. These characters are potentially useful for distinguishing

Metridia and Pseudocalanus nauplii from other regions, contributing

to the understanding of their role in various ecosystems.

p. Bering Sea and North Pacific Ocean Theme Page (http://www.pmel.

noaa.gov/bering):

Funding from BS FOCI was used to support the creation of a Bering

Sea and North Pacific Ocean Theme Page. The theme page provides

pointers to information and images generated by NOAA, universities,

and other governmental sources and other information grouped by scientific discipline. This page includes links to up-to-date satellite imagery, new research, and educational material related to the Northern
160 S.A. Macklin (ed.)

Pacific Ocean and the Bering Sea. Efforts included the design of the

pages, location of resources to be included in the pages, prototyping

of the theme page family of pages, interaction with PMEL and AFSC

researchers to refine the page, and production of a public version of the

page that became available in June 1997. The primary page includes

sub-pages covering physical and biological sciences in the North Pacific;

research, monitoring, and assessment information; a subject index; and

a What’s New section providing direct access to both new links on the

pages and information on technical changes in the pages. With completion of the public version of the page, efforts turned to development

of data access routines and pages to bolster data access. Routines for

the display of drifter data and for the overlaying of biological data on

physical oceanographic properties have been developed. The drifter

data page allows selection of a single drifter or a set of drifters, and

plotting of either the current location or the history of the drifter. Development of data displays for biological data has included: design of

EPIC data formats for biological bottle data; development of routines

to take bottle data from original database format and transform it

into EPIC format files; routines to locate concurrent bottle and CTD

data files; and routines to plot biological data as an overlay on a plot of

physical data. Information is also available on user access to the theme

page; during winter 1998there were about 20,000 hits each month on

the site. An up-to-date summary of access statistics is available from

http://corona.pmel.noaa.gov/∼rees/stats/bering/no pmel.

5.4 References

Bailey, K.M., D. Powers, J. Quattro, G. Villa, A. Nishimura, J. Traynor, and G.

Walters (1998): Population ecology and structural dynamics of walleye pollock,

Theragra chalcogramma. In Dynamics of the Bering Sea, Loughlin, T.R., and

K. Ohtani (eds.), Alaska Sea Grant Press, in press.

Brodeur, R.D., J.M. Napp, M.T. Wilson, S.J. Bograd, E.D. Cokelet, and J.D. Schumacher (1996): Acoustic detection of mesoscale biophysical features in the Shelikof Sea valley, and their relevance to pollock larvae in the Gulf of Alaska. Fish.

Oceanogr., 5 (Suppl. 1), 71–80.

Brooker, A.L., D. Cook, P. Bentzen, J.M. Wright, and R.W. Doyle (1994): Organization of microsatellites differ between mammals and cold-water teleost fishes.

Can. J. Fish. Aquat. Sci., 51, 1959–1966.

Chapman, W.L., and J.E. Walsh (1993): Recent variations of sea ice and air temperature in high latitudes. Bull. Am. Meteorol. Soc., 74, 33–47.

Cokelet, E.D., J.M. Napp, and D.M. Dougherty: Acoustic Doppler current profiler backscatter calibration for Bering Sea zooplankton. ICES J. Mar. Sci., in

preparation.

Cokelet, E.D., M.L. Schall, and D. Dougherty (1996): ADCP-referenced geostrophic

circulation in the Bering Sea basin. J. Phys. Oceanogr., 26, 1113–1128.

Cokelet, E.D., and P.J. Stabeno (1997): Mooring observations of the thermal structure, salinity and currents in the SE Bering Sea basin. J. Geophys. Res., 102,

22,947–22,964.

Davis, R.F., G. Lazin, J. Bartlett, A. Ciotti, and P. Stabeno (1997a): Remote

sensing of a pigment patch in the southeastern Bering Sea. In Ocean Optics

XIII, Proc. Soc. Photo-Opt. Instrum. Eng., 2963, 654–657.
Bering Sea FOCI Final Report 161

Davis, R.F., C.C. Moore, J.R.V. Zaneveld, and J.M. Napp (1997b): Reducing the

effects of fouling on chlorophyll estimates derived from long-term deployment

of optical instruments. J. Geophys. Res., 102, 5851–5856.

Francis, R.C., R. Merrick, K. Aydin, and S.M. Bollens (1998): Modeling and management of the Bering Sea ecosystem. In The Bering Sea: Physical, Chemical

and Biological Dynamics Loughlin, T.R., and K. Ohtani (eds.), University of

Alaska Sea Grant Press, in press.

Greenlaw, C.F. (1979): Acoustical estimation of zooplankton populations. Limnol.

Oceanogr., 24, 226–242.

Howell-Kubler, A.N., E.J. Lessard, and J.M. Napp (1996): Springtime protozoan

abundance and biomass in the southeastern Bering Sea and Shelikof Strait,

Alaska: Its [sic] potential role as prey for planktivorous fish larvae. J. Plankton

Res., 18, 731–745.

Lessard, E.J., M.P. Martin, and D.J.S. Montagnes (1996): A new method for livestaining protozoa with DAPI for use as a tracer of ingestion by walleye pollock

(Theragra chalcogramma) larvae. Mar. Ecol. Prog. Ser., 204, 43–57.

Liu, A.K., C.Y. Peng, and S.Y.-S. Chang (1997): Wavelet analysis of satellite images

for Coastal Watch. IEEE J. Oceanic Eng., 22(1), 9–17.

Liu, A.K., C.Y. Peng, and J.D. Schumacher (1994): Wave-current interaction study

in the Gulf of Alaska for detection of eddies by SAR. J. Geophys. Res., 99,

10,075–10,085.

Mitson, R.B., Y. Simard, and C. Goss (1996): Use of a two-frequency algorithm

to determine size and abundance of plankton in three widely spaced locations.

ICES J. Mar. Sci., 53, 209–215.

Napp, J. M., R.D. Brodeur, D. Demer, R. Hewitt, J.D. Schumacher, P.J. Stabeno,

and G.L. Hunt, Jr.: Acoustic determination of zooplankton and nekton distributions at tidally generated shelf fronts in the eastern Bering Sea. Mar. Ecol.

Prog. Ser., submitted.

Overland, J.E., M.C. Spillane, H.E. Hurlburt, and A.J. Wallcraft (1994): A numerical study of the circulation of the Bering Sea basin and exchange with the

North Pacific Ocean. J. Phys. Oceanogr., 24, 736–758.

Reed, R.K., and P.J. Stabeno: The Aleutian North Slope Current. In Physical

Characteristics of the Bering Sea. In Dynamics of the Bering, Loughlin, T.R.,

and K. Ohtani (eds.), Alaska Sea Grant Press, in press.

Severin, K.P., J. Carroll, and B.L. Norcross (1995): Electron microprobe analysis of

juvenile walleye pollock, Theragra chalcogramma, otoliths from Alaska: A pilot

stock separation study. Env. Biol. Fish., 43, 269–283.

Siefert, D.L.W. (1998): Distinguishing between Stage I and Stage II nauplii of the

copepods Metridia and Pseudocalanus from the Bering Sea. J. Plankton Res.,

20, 1061–1072.

Spring, S. (1996): Swimming behavior of walleye pollock larvae Theragra chalcogramma in relation to zooplankton. Master of Science Thesis, University of

Washington, Seattle.

Stabeno, P.J., J.J. Cullen, R.F. Davis, and R. Leben: Dynamics and productivity

of an eddy in the southeastern Bering Sea. J. Geophys. Res., in preparation.

Stabeno, P.J., and R.K. Reed (1994): Circulation in the Bering Sea basin observed

by satellite-tracked drifters: 1986–1993. J. Phys. Oceanogr., 24, 848–854.

Theilacker, G.H., and W. Shen (1993a): Calibrating starvation-induced stress in

larval fish using flow cytometry. Am. Fish. Soc. Symp., 14, 85–94.

Theilacker, G.H., and W. Shen (1993b): Fish larval condition analyzed using flow

cytometry. In Physiological and Biochemical Aspects of Fish Development,

Walther, B.T., and H.J. Fyhn (eds.), Norway: University of Bergen, 346–355.

Theilacker, G.H., K.M. Bailey, M.F. Canino, and S.M. Porter (1996): Variations in
162 S.A. Macklin (ed.)

larval walleye pollock feeding and condition: A synthesis. Fish. Oceanogr., 5,

112–123.

Villa, G.W., and D.A. Powers: Stock structure of walleye pollock, Theragra chalcogramma, in the Bering Sea region based on nuclear microsatellites. Env. Biol.

Fish, in press.

Wyllie-Echeverria, T. (1996): The relationship between the distribution of one-yearold pollock and sea ice characteristics. In Ecology of Juvenile Walleye Pollock,

Theragra chalcogramma. NOAA Tech. Report., NMFS 126, 47–56.
Bering Sea FOCI Final Report 163

Part 6

Bering Sea FOCI Publication List

Bailey, K.M., 1997: Structural ecology of marine flatfish populations. J. Sea Res.,

37, 269–280.

Bailey, K.M., W.S. Grant, T. Quinn, and P. Bentzen: Population ecology of walleye

pollock. Advances in Marine Biology, submitted.

Bailey, K.M., D. Powers, J. Quattro, G. Villa, A. Nishimura, J. Traynor, and G.

Walters: Population ecology and structural dynamics of walleye pollock, Theragra chalcogramma. In: The Bering Sea: Physical, Chemical and Biological

Dynamics, T.R. Loughlin and K. Ohtani (eds.), University of Alaska Sea Grant,

Fairbanks, Alaska 99775, in press.

Bailey, K.M., P. Stabeno, and D. Powers, 1997: The role of larval retention and

transport features in mortality and gene flow of walleye pollock, Theragra

chalcogramma. J. Fish Biol., 51, 135–154.

Bollens, S.M., B.W. Frost, H.R. Schwaninger, C.S. Davis, K.J. Way, and M.C.

Landsteiner, 1992: Seasonal plankton cycles in a temperate fjord, and comments

on the match-mismatch hypothesis. J. Plankton Res., 14, 1279–1305.

Bond, N.A., J.E. Overland, and P. Turet, 1994: Spatial and temporal characteristics

of the wind forcing of the Bering Sea. J. Clim., 7, 1119–1130.

Brodeur, R.D. 1998: In situ observations of the association between juvenile fishes

and scyphomedusae in the Bering Sea. Mar. Ecol. Prog. Ser., 163, 11–20.

Brodeur, R.D., M.T. Wilson, and L. Ciannelli: Spatial and temporal variability in

feeding and condition of age-0 walleye pollock in frontal regions of the Bering

Sea. ICES J. Mar. Sci., in press.

Brodeur, R.D., M.T. Wilson, J.M. Napp, P.J. Stabeno, and S. Salo, 1997: Distribution of juvenile pollock relative to frontal structure near the Pribilof Islands,

Bering Sea. Proc. Int. Symp. on the Role of Forage Fishes in Marine Ecosystems, Alaska Sea Grant AK-97-01, 573–589.

Brodeur, R.D., M.T. Wilson, G.E. Walters, and I. Melnikov: Forage fishes in the

Bering Sea: Distribution, species associations, and biomass trends. In: The

Bering Sea: Physical, Chemical and Biological Dynamics, T.R. Loughlin and

K. Ohtani (eds.), University of Alaska Sea Grant, Fairbanks, Alaska 99775, in

press.

Cokelet, E.D., M.L. Schall, and D. Dougherty, 1996: ADCP-referenced geostrophic

circulation in the Bering Sea basin. J. Phys. Oceanogr., 26(7), 1113–1128.

Cokelet, E.D., and P.J. Stabeno, 1997: Mooring observations of the thermal structure, salinity and currents in the SE Bering Sea basin. J. Geophys. Res., 102,

22,947–22,964.

Cullen, J.J., A.M. Ciotti, F. Davis, and M.R. Lewis, 1997: Optical detection and

assessment of algal blooms. Limnol. Oceanogr., 42(5, part 2), 1223–1239.

Davis, R.F., J.J. Cullen, and A.M. Ciotti, Ocean color of the southeastern Bering  ́

Sea: Remotely sensed and in situ results. Inter. J. Rem. Sens., in preparation.

Davis, R.F., G. Lazin, J. Bartlett, A Ciotti, and P. Stabeno, 1997: Remote sensing

of a pigment patch in the southeastern Bering Sea. In: Ocean Optics XIII,

Proc. Soc. Photo-Opt. Instrum. Eng., 2963, 654–657.

Davis, R.F., C.C. Moore, J.R.V. Zaneveld, and J.M. Napp: Reducing the effects of

fouling on chlorophyll estimates derived from long-term deployment of optical

instruments. J. Geophys. Res., in press.

Francis, R.C., R. Merrick, K. Aydin, and S.M. Bollens: Modeling and management

of the Bering Sea ecosystem. In: The Bering Sea: Physical, Chemical and
164 S.A. Macklin (ed.)

Biological Dynamics, T.R. Loughlin and K. Ohtani (eds.), University of Alaska

Sea Grant, Fairbanks, Alaska 99775, in press.

Hillgruber, N., L.J. Haldorson, and A.J. Paul, 1995: Feeding selectivity of larval

walleye pollock Theragra chalcogramma in the oceanic domain of the Bering

Sea. Mar. Ecol., 120, 1–10.

Howell-Kubler, A.N., E.J. Lessard, and J.M. Napp, 1996: Springtime protozoan

abundance and biomass in the southeastern Bering Sea and Shelikof Strait,

Alaska: Its [sic] potential role as prey for planktivorous fish larvae. J. Plankton

Res., 18, 731–745.

Kendall, A.W., Jr.: Fisheries Oceanography Coordinated Investigations (FOCI) in

the Bering Sea. Presented at: Comparisons between the Oyashio Region and

the Bering Sea Ecosystems, Hokkaido University, January 1998. Mem. Fac.

Fish. Hokkaido University, in press.

Lang, G.M., R.D. Brodeur, J.M. Napp, and R. Schabetsberger: Variation in groundfish predation on juvenile walleye pollock relative to hydrographic structure near

the Pribilof Islands, Alaska. ICES J. Mar. Sci., in press.

Lazin, G., R.F. Davis, A.M. Ciotti, and M.R. Lewis, 1997: Ocean color measurements from low flying aircraft: Atmospheric and surface glint correction. In:

Ocean Optics XIII, Proc. Soc. Photo-Opt. Instrum. Eng., 2963, 703–707.

Lessard, E.J., M.P. Martin, and D.J.S. Montagnes, 1996: A new method for livestaining protozoa with DAPI for use as a tracer of ingestion by walleye pollock

(Theragra chalcogramma) larvae. Mar. Ecol. Prog. Ser., 204, 43–57.

Liu, A.K., C.Y. Peng, and S.Y.-S. Chang, 1997: Wavelet analysis of satellite images

for coastal watch. IEEE J. Oceanic Eng., 22, 9–17.

Luchin, V.A., V.A. Menovschikov, V.M. Lavrientiev, and R.K. Reed: Thermohaline

structure and water masses in the Bering Sea. In: The Bering Sea: Physical,

Chemical and Biological Dynamics, T.R. Loughlin and K. Ohtani (eds.), University of Alaska Sea Grant, Fairbanks, Alaska 99775, in press.

Macklin, S.A.: Bering Sea FOCI. In: The Bering Sea: Physical, Chemical and

Biological Dynamics, T.R. Loughlin and K. Ohtani (eds.), University of Alaska

Sea Grant, Fairbanks, Alaska 99775, in press.

Megrey, B.A., 1991: Pollock recruitment and reproduction. In: Discussion Summaries from the International Workshop on Bering Sea Pollock Stock Assessment; J.E. Pearce (compiler), AFSC Processed Report 91-06, NOAA/NMFS,

Seattle, WA 98115, 53 pp.

Napp, J. M., R.D. Brodeur, D. Demer, R. Hewitt, J.D. Schumacher, P.J. Stabeno,

and G.L. Hunt, Jr.: Acoustic determination of zooplankton and nekton distributions at tidally generated shelf fronts in the eastern Bering Sea. Mar. Ecol.

Prog. Ser., submitted.

Napp, J. M., A.W. Kendall, Jr., and J.D. Schumacher: Biophysical processes relevant to recruitment dynamics of walleye pollock (Theragra chalcogramma) in

the eastern Bering Sea. Fish. Oceanogr., submitted.

Napp, J.M., K. Mier, and M.K. Cohen: Estimation of larval fish prey volume:

Mensuration formulae for copepod nauplii. J. Plankton Res., submitted.

Overland, J.E., and L.H. Kantha: Mixing and stratification on the Bering Sea shelf.

J. Geophys. Res., submitted.

Overland, J.E., M.C. Spillane, H.E. Hurlburt, and A.J. Wallcraft, 1994: A numerical

study of the circulation of the Bering Sea basin and exchange with the North

Pacific Ocean. J. Phys. Oceanogr., 24, 736–758.

Overland, J.E., P.J. Stabeno, and S.A. Salo, 1996: Direct evidence for northward

flow on the northwestern Bering Sea shelf. J. Geophys. Res., 101, 8971–8976.

Paul, A.J., J.M. Paul, and K.O. Coyle, 1996: Abundance and taxa composition of

copepod nauplii over southeastern Bering Sea deep water spawning grounds of

walleye pollock, Theragra chalcogramma. Crustaceana, 69, 494–508.
Bering Sea FOCI Final Report 165

Pinchuk, A.I., 1997: Early life history of Metridia pacifica Brodsky (Copepoda:

Calanoida) from the southeastern Bering Sea and Gulf of Alaska. M.S. Thesis,

University of Alaska Fairbanks, 65 pp.

Pinchuk, A.I., 1997: Naupliar development of Metridia pacifica Brodsky, 150 (Copepoda: Calanoida) reared in the laboratory. J. Crustacean Biol., 17, 343–351.

Pinchuk, A.I., and A.J. Paul (1998): Growth of Metridia pacifica (Copepoda:calanoida)

nauplii in the laboratory. Plankton Biol. Ecol., 45(2) (in press).

Reed, R.K., 1995: On geostrophic reference levels in the Bering Sea basin. J.

Oceanogr., 51, 489–498.

Reed, R.K., 1995: On the variable subsurface environment of fish stocks in the

Bering Sea. Fish. Oceanogr., 4, 317–323.

Reed, R.K., 1995: Water properties over the Bering Sea shelf: Climatology and

variations. NOAA Tech. Report ERL 452-PMEL 42, 15 pp.

Reed, R.K.: Confirmation of a convoluted flow over the southeastern Bering Sea

shelf. Cont. Shelf Res., in press.

Reed, R.K., G.V. Khen, P.J. Stabeno, and A.V. Verkhunov, 1993: Water properties

and flow over the deep Bering Sea basin, summer 1991. Deep-Sea Res., 40,

2325–2334.

Reed, R.K., J.D. Schumacher, C.H. Pease, P.J. Stabeno, A.W. Kendall, Jr., and

P. Dell’Arciprete, 1994: Bering Sea circulation explored. Eos Trans. AGU, 75,

342.

Reed, R.K., and P.J. Stabeno, 1993: The recent return of the Alaskan Stream to

Near Strait. J. Mar. Res., 51, 515–527.

Reed, R.K., and P.J. Stabeno, 1994: Flow along and across the Aleutian ridge. J.

Mar. Res., 52, 639–648.

Reed, R.K., and P.J. Stabeno, 1996: On the climatological mean circulation over

the eastern Bering Sea shelf. Cont. Shelf Res., 16, 1297–1305.

Reed, R.K., and P.J. Stabeno, 1997: Long-term measurements of flow near the

Aleutian Islands. J. Mar. Res., 55, 565–575.

Reed, R.K., and P.J. Stabeno: The Aleutian North Slope Current. In: The Bering

Sea: Physical, Chemical and Biological Dynamics, T.R. Loughlin and K. Ohtani

(eds.), University of Alaska Sea Grant, Fairbanks, Alaska 99775, in press.

Reed, R.K., A.V. Verkhunov, G.V. Khen, E.D. Cokelet, J.E. Overland, and T.E.

Whitledge, 1992: Recent U.S.–U.S.S.R. cruise in Bering Sea. Eos Trans. AGU,

73, 16, p. 184.

Roach, A.T., K. Aagaard, C.H. Pease, S.A. Salo, T. Weingartner, M. Kulakov,

and V. Pavlov, 1995: Direct measurements of transport and water properties

through Bering Strait. J. Geophys. Res., 100, 18,443–18,457.

Royer, T.C., and P.J. Stabeno: Polar Ocean Boundaries. The Sea, Vol. 10, in press.

Schumacher, J. D., and V. Alexander: Variability and role of the physical environment in the Bering Sea ecosystem. In: The Bering Sea: Physical, Chemical and

Biological Dynamics, T.R. Loughlin and K. Ohtani (eds.), University of Alaska

Sea Grant, Fairbanks, Alaska 99775, in press.

Schumacher, J.D., and R.K. Reed, 1992: Characteristics of currents over the continental slope of the eastern Bering Sea. J. Geophys. Res., 97, 9423–9433.

Schumacher, J.D., and P.J. Stabeno, 1994: Ubiquitous eddies of the eastern Bering

Sea and their coincidence with concentrations of larval pollock. Fish. Oceanogr.,

3, 182–190.

Schumacher, J.D., and P.J. Stabeno: The continental shelf of the Bering Sea. The

Sea, Vol. 10, in press.

Schumacher, J.D., P.J. Stabeno, N.A. Bond, and J.M. Napp, 1998: Ecosystem

anomalies in the eastern Bering Sea during 1997. NPAFC Workshop, in press.

Severin, K.P., J. Carroll, and B.L. Norcross, 1995: Electron microprobe analysis of
166 S.A. Macklin (ed.)

juvenile walleye pollock, Theragra chalcogramma, otoliths from Alaska: A pilot

stock separation study. Env. Biol. Fish., 43, 269–283.

Siefert, D.L.W., 1998: Distinguishing between stage I and stage II nauplii of the

copepods Metridia and Pseudocalanus from the Bering Sea. J. Plankton Res.,

20, 1061–1072.

Spring, S., 1997: Swimming behavior of walleye pollock larvae Theragra chalcogramma in relation to food. M.S. Thesis, University of Washington, Seattle,

Washington 98195, 123 pp.

Stabeno, P.J., J. Napp, and R. Reed: Magnitude and time scales of inflow through

Unimak Pass, Alaska. Geophys. Res. Lett., in preparation.

Stabeno, P.J., and R.K. Reed, 1992: A major circulation anomaly in the western

Bering Sea. Geophys. Res. Lett., 19, 1671–1674.

Stabeno, P.J., and R.K. Reed, 1994: Circulation in the Bering Sea basin observed

by satellite-tracked drifters: 1986–1993. J. Phys. Oceanogr., 24, 848–854.

Stabeno, P.J., and R.K. Reed: Drifters on the Bering Sea shelf: Kinematics and

diffusivity. J. Phys. Oceanogr., in preparation.

Stabeno, P.J., R.K. Reed, and J.E. Overland, 1994: Lagrangian measurements in

the Kamchatka Current and Oyashio. J. Oceanogr., 50, 653–662.

Stabeno, P.J., J.D. Schumacher, R.F. Davis, and J.M. Napp, 1998: Under-ice observations of water column temperature, salinity and spring phytoplankton dynamics: Eastern Bering Sea shelf, 1995. J. Mar. Res., 56, 239–255.

Stabeno, P.J., J.D. Schumacher, and K. Ohtani: Overview of the Bering Sea. In:

The Bering Sea: Physical, Chemical and Biological Dynamics, T.R. Loughlin

and K. Ohtani (eds.), University of Alaska Sea Grant, Fairbanks, Alaska 99775,

in press.

Stabeno, P.J., J.D. Schumacher, S.A. Salo, G.L. Hunt, and M. Flint: The physical

environment around the Pribilof Islands. In: The Bering Sea: Physical, Chemical and Biological Dynamics, T.R. Loughlin and K. Ohtani (eds.), University

of Alaska Sea Grant, Fairbanks, Alaska 99775, in press.

Sugisaki, H., R. Brodeur, and J. Napp: Summer distribution and abundance of

macrozooplankton in the western Gulf of Alaska and the Bering Sea. Proceedings of Comparison Between the Oyashio Region and Bering Sea Ecosystem

Symposium, submitted.

Swartzman, G., R. Brodeur, J. Napp, D. Walsh, R. Hewitt, D. Demer, G. Hunt,

and E. Logerwell: Relating predator and prey spatial distributions in the Bering

Sea using acoustic backscatter data. Can. J. Fish. Aquat. Sci., in press.

U.S. GLOBEC, 1996: Report on climate change and carrying capacity planning

meeting. (A.B. Hollowed, ed.; Contributions by R. Brodeur, N. Bond, E.D.

Cokelet, A. Hermann, B. Megrey, J. Napp, J. Overland, R. Reed, J. Schumacher,

P. Stabeno, et al.). U.S. GLOBEC Rep. 15, University of California, Berkeley.

Vance, T., and S.A. Macklin, 1998: What the heck is a coccolithophore? Alaska

Fisherman’s Journal, 21(3), 36–37.

Van Meurs, P., and P. Stabeno: Evidence for episodic on-shelf flow. J. Geophys.

Res., in press.

Villa, G.W., and D.A. Powers: Stock structure of walleye pollock, Theragra chalcogramma, in the Bering Sea region based on nuclear microsatellites. Env. Biol.

Fish., in press.

Wyllie Echeverria, T., 1995: Sea-ice conditions and the distribution of walleye

pollock (Theragra chalcogramma) on the Bering and Chukchi Sea Shelf. Can.

Spec. Pub. Fish. Aquat. Sci., 121, 131–136.

Wyllie Echeverria, T., 1996: The relationship between the distribution of one year

old pollock and sea ice characteristics. NOAA Tech. Report, NOAA NMFS-126,

47–56.
Bering Sea FOCI Final Report 167

Wyllie-Echeverria, T.: Remotely sensed seasonal sea ice and oceanology of the

Bering Sea. In: Satellite Sensing of the North Pacific Ocean, Earth, Ocean and

Space Pty. Ltd., Sydney, Australia, in press.

Wyllie-Echeverria, T., and K. Ohtani: Seasonal sea ice variability in the Bering Sea

ecosystem. In: The Bering Sea: Physical, Chemical and Biological Dynamics,

T.R. Loughlin and K. Ohtani (eds.), University of Alaska Sea Grant, Fairbanks,

Alaska 99775, in press.

Wyllie-Echeverria, T. and W.S. Wooster: Sea ice as an indicator of interannual and

decadal climatic variability in the Bering Sea ecosystem. Fish. Oceanogr., in

press.