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This document is available to the public through:

National Technical Information Service

U.S. Department of Commerce

5285 Port Royal Road

Springfield, VA 22161
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PREFACE

It has been 13 years since the last conference on biotic and abiotic factors affecting

oceanic and estuarine survival of salmon. The proceedings from that meeting, “The Influence of

Ocean Conditions on the Production of Salmonids in the North Pacific,” edited by William

Pearcy (1983), summarized existing information linking oceanic conditions and salmonid

survival, distribution, and abundance. All four work groups at the 1983 meeting emphasized the

need to understand the effects of ocean conditions on salmonid survival, and called for long-term

studies of the marine environment.

Unfortunately, the recommendations from the 1983 meeting have gone largely unheeded.

Although the salmon research community has continued to spend large amounts of time and

funding on freshwater habitat issues, relatively little has been spent on estuarine and marine

salmonid habitat issues. In the meantime, Northwest salmon populations have continued to

decline, with “poor” ocean conditions often being acknowledged as playing some ill-defined

role.

In an effort to once again highlight the importance of estuarine and oceanic residency to

salmon survival and year-class strength, we convened a small group in the summer of 1995 to

begin planning a workshop to bring together scientists whose research addresses some aspect of

this important issue. Providing further impetus to our efforts were several recent reports,

including the National Research Council’s “Upstream: Salmon and Society in the Pacific

Northwest” (1996) and the Snake River Salmon Recovery Team’s “Final Recommendations for

the National Marine Fisheries Service,” which have highlighted the need to fully understand

salmonid estuarine and marine life histories—not just because these environments are where

salmonids spend most of their lives, but also because substantial mortalities occur there, and

rigorous evaluations of freshwater salmonid enhancement projects require information on

estuarine and ocean survival.

The workshop consisted of 25 presentations, organized in the following six sessions:

1) selected aspects of salmonid life histories

2) interannual variations in Northeast Pacific marine habitats and the effects on marine

survival of salmonids

3) decadal variations in Northeast Pacific marine habitats and the effects on marine

survival of salmonids

4) processes and mechanisms in estuarine habitats

5) processes and mechanisms in nearshore coastal habitats

6) processes and mechanisms in offshore marine habitats

On the final day of the workshop, four working groups were organized to identify and discuss

critical research needs, formulate testable hypotheses, and identify potential research strategies to

enhance understanding of the role of estuarine and oceanic habitats in salmonid survival.
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Since the four work groups met independently, their results are presented in slightly different

formats.

As with any scientific meeting, the ultimate success depended largely on the thoughtful

planning of the steering committee. For the 1996 Newport workshop, “Estuarine and Ocean

Survival of Northeast Pacific Salmon,” the steering committee was composed of Dr. George

Boehlert of NMFS’s Southwest Fisheries Science Center, Dr. Robert Francis of the University of

Washington, Dr. Steve Ignell of NMFS’s Alaska Fisheries Science Center, Dr. William Pearcy of

Oregon State University, and Drs. Michael Schiewe and William Peterson, and Mr. Robert

Emmett of the Northwest Fisheries Science Center. Drs. William Peterson, Richard Brodeur,

Michael Bradford, Colin Levings, Steve Ignell, and Bruce McCain, and Ms. Kate Myers served

as chairs and rapporteurs for the working groups. Finally, Ms. Sharon Damkaer and Dr. David

Damkaer greatly assisted with compiling, editing, and reviewing the manuscripts in these

proceedings.

Although it has taken 13 years to reconvene a conference on oceanic and estuarine

survival of salmon, the results perhaps justify the wait. More than 140 scientists, representing

disciplines ranging from fisheries ecology to population dynamics, and physical and biological

oceanography to climatology, spent three intellectually stimulating days listening to papers,

engaging in discussion, and planning future collaborations. To all the participants, we extend our

sincere thanks.

Robert L. Emmett and Michael H. Schiewe

Northwest Fisheries Science Center
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WELCOME

I take great pleasure in welcoming you to this conference on estuarine and ocean

survival of northwestern Pacific salmon. Both the topic of this conference and its location in

Newport are very significant to the Northwest Fisheries Science Center (NWFSC). I think

most of you know that just a few minutes south of here is the campus of Oregon State

University’s Hatfield Marine Science Center. The Hatfield Center also houses laboratories of

the National Marine Fisheries Service (NMFS), the Environmental Protection Agency, and

the Oregon Department of Fish and Wildlife. This setting provides an ideal opportunity to

undertake cooperative research programs among the federal, state, and university scientists.

We began capitalizing on that potential about a year ago, when we transferred a few of our

Seattle researchers to the Newport laboratory. We have also been very fortunate to hire a

small number of highly qualified scientists to work on two new research programs at

Newport. The first is the west coast groundfish ecology and assessment program. The second

is a program to develop research strategies on estuarine and ocean survival of both marine

and anadromous fishes.

I am very pleased to be here because this conference allows scientists from different

institutions and different disciplines to come together to discuss important issues regarding

salmon survival. I think all of you are aware of the national attention focused on the declining

salmon stocks in the Pacific Northwest. The salmon problem encompasses the entire West

Coast. There is a great deal of concern that we scientists are focusing considerably more

attention on certain problems and not enough on others. One of the areas that requires good

scientific planning and effort is the understanding of the factors that affect estuarine and

ocean survival of salmon.

Salmon, in the course of their natural life cycle, originate in fresh water, pass through

estuaries, adapt to salt water, and travel long distances in the ocean before returning to their

natal stream to spawn. This life-history strategy is very complex and demanding for the

species to maintain, as well as difficult for the scientists to study. The salmon species also

has to cope with a number of natural and human-induced habitat changes. When these

anthropogenic changes are superimposed on natural upheavals, they cause major impacts on

salmon survival. As a result, on the West Coast where environmental and anthropogenic

changes have been catastrophic, we are seeing considerable decline in many salmonid

populations.

Considering all of the stresses that we are putting on salmon and their habitats, it is

amazing that we still have any salmon left. Nevertheless, I believe that with a combination of

dedicated scientific effort, wise environmental effort, and good management, we can mitigate

at least some of the major stresses that salmon are facing. Most of the attention so far has

been on the alterations in fresh water, partly because the changes are much more obvious and

easier to study and correct. However, it has become very clear that we need to focus on and

develop considerable information about all stages and geographic phases of the salmon life

history.
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The importance of this information has been emphasized in the Snake River Recovery

Team recommendations, in the NMFS-proposed Snake River Salmon Recovery Plan, and in

the National Research Council’s report. This is the right time for us to come together. I’m

very thankful to Mike Schiewe and the steering committee, who have worked for the last 6-8

months to develop this agenda and to bring you all together here. I think it is time for us to

identify the areas in which we presently have a lack of information and understanding, and

what actions we should undertake collectively for the next few years. So I’m looking forward

to your presentations and to the directions for new research that you will recommend. I’m

very pleased that NMFS is able to sponsor this conference along with our colleagues at

Oregon State University — I am a strong believer in multi-disciplinary efforts to address and

develop innovative research strategies.

My own experience as a scientist, working for about 20 years on marine pollution

issues, has shown that success has always occurred when scientists from different disciplines

come together in somewhat untraditional alliances. I hope that the people who study natural

processes, those who study anthropogenic stress, those who study biology, and those who

study toxicology can come together. I think this is a good opportunity to develop some

innovative strategies and a collaborative plan that we can all pursue for the next few years to

come.

Thank you very much.

Usha Varanasi, Ph.D.
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KEYNOTE ADDRESS: SALMON OCEANOGRAPHY?

Warren S. Wooster

School of Marine Affairs

University of Washington

3707 Brooklyn Ave. N.E.

Seattle, WA 98105-6715

The last time I was in Newport, in 1983, was for a workshop on the influence of

ocean conditions on the production of salmonids in the North Pacific. It arose from the idea

that the environment in which salmon spend their oceanic years had some important effect on

their survival and growth. At the time, we thought that interannual variability was the most

important frequency—hence our book from a preceding workshop on nonsalmonid species

was called From Year to Year. But since then, as today’s lectures have made clear, many

have come to believe that longer scales, decadal and beyond, are probably more important.

The preface to the 1983 salmon workshop report speaks of the devastating effects of

the 1982-83 Niño event on ocean catches of coho and chinook salmon (Oncorhynchus

kisutch and O. tshawytscha) off Oregon and Washington. More recently, I have even heard El

Niño described as a “catastrophe.” Like hurricanes and earthquakes perhaps, El Niño is only

a catastrophe to the extent that it negatively affects humans. Otherwise, it is a particular

feature of natural variability and may be as beneficial as it is harmful to the marine

ecosystems that it influences. For example, salmon biologists have been forced since 1983 to

contemplate the medium in which their favorite fish spend a critical part of their life history.

Of course, that has not been sufficient to turn all salmon biologists into fishery

oceanographers overnight.

When I came to the University of Washington (UW) nearly 20 years ago, I almost fell

into the chasm that lay between Fisheries and Oceanography. It was my impression then that

the College of Fisheries was interested mostly in salmon and oysters—not a bad combination

if you are hungry, but not really representative of the broad scope of contemporary fishery

problems. There was little interaction with the Department of Oceanography, which stood

aloof from such messy problems. In contrast, I had spent much of my career at an institution

on the edge of a pelagic realm, where interactions between fish and their environment were

accepted as an article of faith, at least after Harold Sverdrup and Elton Sette had cooked up

what became CalCOFI (California Cooperative Oceanic Fisheries Investigations), a program

in which fishery scientists and oceanographers have comfortably cohabited for nearly 50

years.

Of course, there can be too much of a good thing. El Niño has become a convenient

deus ex machina for all sorts of unexplained events, a curious viewpoint for those who

normally see all stock variations as caused by man. In 1982-83, I was asked what El Niño

would mean for salmon returns—I ventured a guess that the effect would be similar to that of

the 1957-58 event, but I was left with the impression that no one had paid much attention to
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that. I tend to see El Niño not as some sort of plague but rather as an important climatic

signal that arises in the equatorial Pacific Ocean and sometimes extends into the subarctic

Pacific, even into the Bering Sea, and in extra-tropical latitudes is usually associated with

decreased upwelling, warming, and deeper thermoclines. These in turn influence primary and

secondary production, distribution of both plankton and nekton, and growth and mortality of

higher level carnivores, including salmon.

But El Niño is not the only influence on these factors, and in the case of fish that are

harvested, the effects of fishing, not only on target stocks, but on their prey, predators, and

competitors, have also to be taken into account. It is my impression that no one really

understands how changes, however induced, in one important component of an oceanic

ecosystem trickle down or bubble up to affect other components. The question comes to a

head in what has been called the carrying capacity problem.

With the increase in the number and output of salmon hatcheries around the North

Pacific rim, and with the observation of reduced growth (smaller size at age) of returning

salmon, the question arises, “Is there a finite carrying capacity for salmon (and other high

trophic level, pelagic carnivores) in the subarctic Pacific, and is it in danger of being

exceeded?” A related question concerns whether carrying capacity is a constant, as tends to

be assumed in the case of marine mammals, or whether it changes in response to climate

variations. These questions led PICES (an international North Pacific organization

comprising Canada, China, Japan, Korea, Russia, and the United States), in 1993, to initiate

development of a GLOBEC program on Climate Change and Carrying Capacity, the socalled CCCC (four Cs) program.

From the beginning, considerable controversy arose over the definition of the term

“carrying capacity.” For purists, it was “k” in the exponential growth curve, what I call the

“bugs in a bottle” approach, and could not be extended to ecosystems. Much of the thinking

on these matters comes from terrestrial or other enclosed systems (e.g., lakes) and does not fit

relatively open-ended systems such as those in the ocean. The debates led ultimately to a

definition that I, at least, am comfortable with: “Carrying capacity for a given population is

considered to be the limiting size of that population that can be supported by an ecosystem

over a period of time and under a given set of environmental conditions.”

The carrying capacity problem is a subset of a grander scientific question: “How are

marine ecosystems of the subarctic Pacific Ocean affected over periods of months to

centuries by changes in the physical environment, by interactions among components of the

ecosystems, and by human activities?”

So how do you study such a vast problem? People find it difficult to think freely

about this question because of the funding situations in which scientists here and in most

other countries find themselves. Thinking is constrained by the perception that only limited

resources are available to support such studies. Without new funding, the only solution is to

reprogram existing funds, a prospect that strikes terror into most bureaucracies and causes

them to develop elaborate defensive strategies. While some coastal programs are already
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funded and under way, studies of the open subarctic Pacific Ocean, the main feeding ground

for most salmon stocks, are much more difficult both to design and to fund.

Two relatively inexpensive approaches are probably the ways to begin, retrospective

studies and modeling/theoretical studies. These are needed both to frame hypotheses and to

design process studies and monitoring efforts. PICES is holding a CCCC Workshop on

Conceptual/Theoretical Studies and Model Development in Nemuro, Hokkaido on 23-

28 June 1996 and is convening a one-day symposium on Methods and Findings of

Retrospective Analyses at its Fifth Annual Meeting in Nanaimo, British Columbia in

October. PICES has a Working Group on Monitoring the Subarctic Pacific Ocean and a

Technical Committee on Data Exchange—these will also support the CCCC program. The

other desideratum at this early stage is a network of committees and study groups in which

scientists participate in planning in a systematic way, achieving some sort of coordination

among the different national GLOBEC and GLOBEC-like programs.

Development of an effective scientific program is colored by fishery politics, in the

United States (Alaska vs. the rest of the country) and internationally. Salmon politics seem to

be particularly virulent. In some countries, fishery agencies take the view that all research on

salmon and ecologically related species—that is, everything else—is their exclusive property.

Perhaps in those countries, fishery science is intimately linked with the other disciplines

necessary for ecosystem studies—meteorology and climatology, oceanography of the several

flavors (physical, chemical, biological), and ecology in the broader sense—but I have not

seen any evidence of such a happy interdisciplinary, interinstitutional marriage there nor in

most other countries. Yet it seems to me that without such a broad approach, the scientific

questions that underlie those of more immediate interest to management are unlikely to be

resolved.

Of course this tension goes beyond any single country. Many here work for

government agencies charged with managing fisheries or with providing the scientific

assessments used by the managers. Some such people tend to follow the accepted population

dynamics paradigms and to be impatient with those who are more free to challenge them and

to pursue other approaches without the day-to-day responsibilities of management. I

remember hearing the director of one fisheries center refer to those in what I thought of as a

particularly productive and insightful research group as “playing in an intellectual sandbox.”

I spoke earlier of the ancient schism between oceanographers and fishery scientists, and my

experience at UW shows that the chasm remains despite more bridges across and more

student interest in crossing those bridges.

I hope we can emerge from this workshop with the conviction that the scientific

questions relating salmon growth and survival to oceanic and estuarine conditions are

important to oceanographers as well as to fishery scientists, and that study of these questions

calls for a full sharing of ideas and joint action among those who can bring their knowledge

and skills to all facets of the question. Perhaps then we will be ready to celebrate the

development of a field that might reasonably be called “salmon oceanography.”

CHANGES IN OCEAN SURVIVAL OF COHO AND CHINOOK SALMON
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Special Topics in Salmonid Life Histories
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IN THE PACIFIC NORTHWEST

Ray Hilborn and Claribel Coronado

Fisheries Research Institute

University of Washington

Seattle, WA 98195-7980

Abundance of salmon has fluctuated greatly. Figure 1 shows the fluctuation in

landings of chinook (Oncorhynchus tshawytscha) and coho (O. kisutch) salmon in the United

States. While we have tended to concentrate on the general decline of chinook and coho

salmon from California to British Columbia, we should not lose sight of the fact that even in

the 1970s there was a general perception that salmon stocks were declining, and in Canada

the Salmonid Enhancement Program was begun with the objective of doubling the number of

salmon.

We want to understand what causes the changes in abundance and what the impacts

of alternative human actions will be. The traditional explanations for changes in salmon

abundance have been the 4-Hs: habitat, harvest, hatcheries, and hydropower. We might

therefore compare the trends in catch, escapement, total run, etc., to human action in one of

these factors, or perhaps in several of them.

It has long been recognized that there is variability in ocean survival of salmon, and

most analyses of human impacts on salmon will treat ocean survival as a form of

uncontrolled noise that confounds the analysis. However, the increasing recognition of largescale changes in ocean conditions suggests that we might need to do more than simply allow

for random ocean survival, but rather try to measure it directly.

Since the early 1970s, there has been an extensive program of tagging Pacific salmon

using coded wire tags. At present, approximately 30 million fish are tagged every year, and

the salmon management agencies on the Pacific coast conduct an extensive tag recovery

program. These data can be used to estimate the survival of tagged fish in the ocean.

Coronado (1995) and Coronado and Hilborn (in prep. (a,b)) have used these data to describe

the changes in ocean survival.

VPA Methodology

We used the estimated recoveries of commercially and recreationally caught fish, and

the estimates of tagged fish in hatchery returns, to calculate the survival rate using virtual

population analyses (VPA) (Hilborn and Walters 1992). For each species we calculated the

estimated survival from time of ocean migration to age 3, the most common age of return for

coho and fall chinook salmon. While VPA does require making an assumption about the rate

of natural mortality for fish in the ocean after age 1, all trends and relative survival are quite
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Figure 1. U.S. landings of coho and chinook salmon, 1922-92.
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insensitive to these assumptions.

Trends

Figures 2, 3, and 4 show the geographic trends in survival for coho and spring and fall

chinook salmon by state and province. In each case, the vertical bars represent standard errors

of the mean computed by using each tag code within the state or province for that year as a

replicate sample. The shaded region represents total hatchery releases.

The trends in survival are both striking and geographically diverse. For instance,

British Columbia coho salmon showed high initial survival in the early 1970s, followed by a

steady decline through the 1980s to a level of about one-third of the initial survival. In

contrast, Washington coho salmon showed steady survivals up until the 1987 brood year and

then a decline after that. For fall chinook salmon, British Columbia and Washington showed

reasonably similar trends, while Oregon and California were quite different. Spring chinook

salmon showed yet a different pattern.

Within geographic regions, there tends to be considerable coherence. For instance,

Figure 5 shows the trends in coho salmon survival for Columbia River hatcheries in

Washington and Oregon. Even though the hatcheries are run by different agencies, the trends,

particularly in the 1980s, are almost identical.

We have performed cluster analysis of survival trends for coho and fall chinook

salmon, and the data tend to cluster by geographic region. We believe these trends reflect the

survival in the early ocean life history of these fish, and this is, in turn, related to the general

oceanographic production regime of the stock.

It is our contention that the survival rate reflects the early ocean survival, and what we

see in the hatchery stocks reflects similar trends in wild fish. While the majority of coded

wire tags are placed on hatchery fish, there has been some tagging of wild stocks. Figure 6

shows the trends in survival of wild and hatchery coho salmon. While far from conclusive,

these data suggest to us that the trends in survival seen in the hatchery fish are likely a

reflection of the survival of wild fish.

Management Implications

This analysis suggests that much of the fluctuation in abundance of chinook and coho

salmon can be explained by changes in ocean survival. This does not mean, however, that we

should ignore human impacts and simply hope for better ocean conditions. The major

purpose of looking at ocean survival is to eliminate this form of variability from analysis

when we consider modification of habitat, harvest, hatcheries, and hydropower.

As an example, we have constructed a simple analysis of optimal harvesting for a
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Figure 2. Survival trends for coho salmon. Line represents survival to age 3; error bars are

the standard error of the mean; shaded area is number of fish released by brood year

x 100,000.
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Figure3. Survival trends for spring chinook salmon. Line represents survival to
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Figure 4. Survival trends for fall chinook salmon. Line represents survival to age 3; error

bars are the standard error of the mean; shaded area is number of fish released by

brood year x 100,000.
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Figure 5.
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Figure 6. Survival trends of hatchery and wild coho salmon in Washington state. Line

represents survival to age 3; error bars indicate standard error of the
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Figure 7. Harvest strategies under different ocean survival rates.
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coho salmon population with constant freshwater conditions, but under two different ocean

regimes (Fig. 7). Here we assume that there is a freshwater carrying capacity and a densityindependent ocean survival. In case 1, we assume a 15% ocean survival, roughly comparable

to the conditions in British Columbia in the early 1970s. The optimal escapement of this

hypothetical stock is 315, and the optimal exploitation rate is 63%. The sustainable yield is

about 500 fish. If the ocean then turns bad and survival drops to 5% (roughly current survival

rates), the sustainable yield drops to 50 fish. The optimum escapement is now only 105, and

the optimum harvest rate is 37%.

Thus, while we cannot control the ocean, we must change our management actions as

ocean conditions change. We suggest that under present ocean conditions there is little if any

sustainable yield for chinook and coho salmon in Oregon, Washington, and British

Columbia. Harvest rates need to be drastically reduced, and we should expect the

escapements to drop. We might choose to maintain escapements at the old levels, but we

should recognize that the reason to do this would be to try to retain a large population size

until ocean conditions improve.

Citations

Coronado, C. 1995. Spatial and temporal factors affecting survival of hatchery-reared

chinook, coho and steelhead in the Pacific Northwest. Ph.D. Thesis, University of

Washington, Seattle, 235 p.

Coronado, C., and R. Hilborn. In prep. (a). Spatial and temporal factors affecting survival in

coho salmon (Oncorhynchus kisutch) in the Pacific Northwest.

Coronado, C., and R. Hilborn. In prep. (b). Spatial and temporal factors affecting survival in

chinook salmon (Oncorhynchus tshawytscha) in the Pacific Northwest.

Hilborn, R., and C. J. Walters. 1992. Quantitative fisheries stock assessment: Choice,

dynamics, and uncertainty. Chapman and Hall, New York, 570 p.
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PARTITIONING MORTALITY IN PACIFIC SALMON

Michael J. Bradford

Freshwater Habitat Science

Department of Fisheries and Oceans

West Vancouver Laboratory

4160 Marine Dr., West Vancouver, BC

V7V 1N6, Canada

Pacific salmon (Oncorhynchus spp.) utilize three or four different habitats during their

life: the subsurface of streams and lakes as embryos and larvae, streams and lakes as young

juveniles, and estuaries and the ocean as older juveniles. Variability in survival in each of

these habitats will contribute to recruitment variation, as will spawner abundance. Here I

briefly review the relative roles of each factor in determining adult abundance.

Parent Stock Size

Pacific salmon are relatively unique among nontropical commercial species in that

their semelparous life history and often simple age structure results in many spawning

populations being dominated by a single cohort of recruits. Thus there is often great variation

in spawner abundance from year to year. Further, the low fecundity of salmon compared to

many marine fish implies that egg-recruit mortality for salmon is much lower (M = 6 to 7;

Bradford 1995) than for many commercial marine species (M = 11 to 14; Koslow 1992).

Interannual variability in mortality is correlated with the mean (Bradford 1992, Bradford and

Cabana 1996), implying that variation in egg-recruit survival in salmon is probably lower

than that for marine fish, depending on the strength and timing of density-dependent

mortality.

The result of these observations is that there is often a relatively strong relationship

between stock and recruitment for Pacific salmon compared to similar data for other species

(Fig. 1), and in many cases recruitment can be forecasted from stock sizes with precision not

available for marine fish. However, because the harvested stock consists only of recruits, and

harvest rates in excess of 70% are common, forecasts of recruitment from stock size are

usually not precise enough for modern-day management. Nonetheless, the point I wish to

highlight is that in many cases a significant portion of variability in adult returns can be

related to parent stock size, irrespective of survival conditions in the various habitats.
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Figure 3. Distribution of mortality (m = 1 ln[S]) among freshwater and marine

environments. Data are from a diverse group of populations: shown are averages

for each species (Bradford 1995).
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Survival in Fresh Water

Salmon use the substrates of rivers and lakes for incubation, and some species use

freshwater habitats for rearing. Survival from egg deposition to fry emergence the following

spring averages about 10%, although there are some data that suggest survival might be

higher for coho (O. kisutch) and chinook (O. tshawytscha) salmon eggs and alevins (Bradford

1995). The coefficient of variation (CV) for interannual survival is about 30%, averaged over

all species. Density effects due to crowding on spawning grounds seem common for species

that spawn in dense aggregations (i.e., pink (O. gorbuscha), sockeye (O. nerka), and chum

(O. keta) salmon; Foerster 1968).

Coho, sockeye, and some chinook salmon populations spend a year or more in fresh

water, and survival rates for this year range from 5% to 25%. In virtually all cases examined,

there is strong evidence for density-dependent population regulation in coho salmon (Table

1), probably due to limited amounts of suitable rearing habitat (Bradford et al. in press).

Density-dependent survival has also been observed in lake-rearing sockeye salmon juveniles

(reviewed by Hume et al. in press). In some cases, the density effects are strong enough to

virtually eliminate the effects of parent stock size on smolt abundance, except at very low

stock size.

While the roles of interannual variation in the physical environment (i.e., weather,

hydrology) and density on survival have been fairly well documented, there are few data sets

that allow analysis of decadal changes in freshwater survival due to low-frequency climate

change or habitat degradation. One exception is the long series of egg-smolt survival rates for

Chilko Lake, B.C. sockeye salmon (Fig. 2). Visual examination of these data suggests an

approximately 15-year cycle in survival, although these data have not been quantitatively

examined. It is not clear whether the overall downward trend in freshwater survival is real or

has resulted from changes in the methods for estimating spawner abundance. Lower survival

rates in the most recent years may also be related to record high spawner abundances that

occurred in the 1980s (Hume et al. in press).

Marine Survival

Most estimates of marine survival are based on smolt abundances made some

distance inland from the sea and, therefore, include mortality during downstream migration

and residence in the estuary. The survival of salmon in the ocean ranges from less than 1% to

more than 10%, depending on the species, the size at ocean entry, and the length of time

spent in the ocean (Bradford 1995). Interannual variability in survival can be quite high (Fig.

2). Although it might be expected that species that enter the ocean at small size are more

susceptible to ocean conditions, and have more variable survival rates, the evidence for this is

equivocal (Bradford 1995).
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Figure 2. Time series of fresh water (CV = 35%) and marine (CV = 59%) survival rates for

Chilko Lake, BC, sockeye salmon. Heavy lines are the 5-year centered running

averages.
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In contrast to the freshwater environment, the evidence for density-dependent survival

in the ocean is not as clear (Pearcy 1992). The analysis of such data is often difficult because

of measurement error (Peterman 1982) and time trends in abundance data, hatchery releases,

and oceanic conditions. In most analyses, density-dependent effects contribute only a small

fraction of the total variability in marine survival rates.

Partitioning Survival

A question that is sometimes posed is what is the relative importance of freshwater,

estuarine, or marine habitats for recruitment variation? It is difficult to comment on the role

of the estuary on variation in adult abundance due to the technical problems in accurately

estimating survival in this habitat, so it is necessary to consider the estuary with the marine

environment.

For the other two major habitats, at the species level, empirical analysis indicates

mortality is roughly equally divided between the two habitats (Fig. 3), and we expect that the

variability in mortality would also be divided similarly (Bradford and Cabana 1996).

Available data suggest that this is true (Bradford 1995), and each habitat contributes

significantly to recruitment variation, although the exact distribution of mortality among

habitats varies by species.

The preceding is based on the naive assumption that mortality in each habitat varies

randomly and is independent of events in the other habitat. The sometimes strong densitydependent mortality that occurs in fresh water means that variation in the number of smolts

produced by a stream or lake is lower than might be expected based on estimates of the

variability in survival or initial egg abundance. In such cases the role of the marine

environment in determining recruitment strength will be greater.

Perhaps of greater interest for conservation purposes is determining the relative roles

of long-term trends in survival in marine and freshwater habitats. A number of recent

analyses have shown decadal trends in adult salmon abundance, which appear to be related to

changes in oceanographic conditions that occur at similar scales (e.g., Hare and Francis

1995). Nonetheless, at the moment it is difficult to apportion these trends in abundance to

changes in survival in the marine or freshwater environment, or to changes in the number of

parent spawners caused by harvest management. The only way to directly address this issue

is with long-term data sets where all major stages of the life cycles are accurately

enumerated. With these data we may be able to determine the effect that long-term changes

in climate have on productivity of both marine and freshwater environments.

Chilko Lake sockeye salmon time series is an example of such data (Fig. 2). From the

smoothed trends in freshwater and marine survival rates there might be some evidence for

interdecadal cycles in survival. However, the cycles (if real) appear to be out of phase with

each other, and there is little correlation in survival between environments. Coupling of
25

freshwater and marine survival rates may be more likely for coastal stocks (e.g., Cooney

et al. 1995).

In summary, partitioning survival to different parts of the salmon’s life cycle is

somewhat scale dependent. At the annual scale, we can generalize that survival and its

variability are roughly equally divided between freshwater and marine habitats. However,

there are only a few instances where we can examine the effects of interdecadal-scale climate

forcing on freshwater and marine survival simultaneously. Such analyses will be difficult

because density-dependent effects and anthropogenic habitat changes in fresh water will tend

to obscure climate effects. Nonetheless, these analyses are essential to correctly interpret

changes in salmon production at decadal or longer scales.

Citations

Bradford, M. J. 1992. Strength and precision of recruitment predictions from the early life

stages of marine fishes. Fish. Bull., U.S. 90:439-453.

Bradford, M. J. 1995. Comparative analysis of Pacific salmon survival rates. Can. J. Fish.

Aquat. Sci. 52:1327-1338.

Bradford, M. J., G. C. Taylor, and J. A. Allan. In press. Empirical review of coho salmon

smolt abundance and the prediction of smolt production at the regional level. Trans.

Am. Fish. Soc.

Bradford, M. J., and G. Cabana. 1996. Interannual variation in stage-specific survival rates

and the causes of recruitment variation. In R. C. Chambers and E. A. Trippel

(editors), Early life history and recruitment in fish populations, p. 597-630. Chapman

and Hall, New York.

Cooney, R. T., T. M. Willette, S. Sharr, D. Sharp, and J. Olson. 1995. The effect of climate

on North Pacific pink salmon (Oncorhynchus gorbuscha) production: Examining

some details of a natural experiment. In R. J. Beamish (editor), Climate change and

northern fish populations, p. 475-482. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Foerster, R. E. 1968. The sockeye salmon. Bull. Fish. Res. Board Can. 162.

Hare, S. R., and R. C. Francis. 1995. Climate change and salmon production in the Northeast

Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations, p. 357-372. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Hume, J. M. B., K. S. Shortreed, and K. F. Morton. In press. Juvenile sockeye rearing

capacity of three lakes in the Fraser River system. Can. J. Fish. Aquat. Sci.
26

Koslow, J. A. 1992. Fecundity and the stock-recruitment relationship. Can. J. Fish. Aquat.

Sci. 49:210-217.

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Univ. Washington Press,

Seattle, 179 p.

Peterman, R. M. 1982. Non-linear relation between smolts and adults in Babine Lake

sockeye populations and implications for other salmon populations. Can. J. Fish.

Aquat. Sci. 39:904-913.
27

GEOGRAPHICAL VARIATION IN LIFE HISTORIES OF SALMONIDS

Laurie Weitkamp, Peggy Busby, and Kathleen Neely

National Marine Fisheries Service

Northwest Fisheries Science Center

Coastal Zone and Estuarine Studies Division

2725 Montlake Boulevard East

Seattle, WA 98112

Pacific salmonids (Oncorhynchus spp.) have complex life histories. They display

considerable inter- and intraspecific variability at all life stages, which results from the

influence of numerous factors. Despite this variability, geographical patterns in some of the

better-studied life stages can provide considerable insight into ecological processes that occur

during estuarine and ocean residency, a period for which little is known. This paper describes

several examples of how life history trait patterns provide information about key questions

concerning estuarine and ocean residence, such as when and why significant mortality

occurs, which fish survive, and how widespread particular patterns are. Estuarine and ocean

residency is just one part of the life cycle, but considerable insight can be gained by viewing

it in the context of the entire life cycle.

A review of data for salmonid populations along the west coast of North America

(from numerous sources including Aro and Shepard 1967, Atkinson et al. 1967, Groot and

Margolis 1991, Weitkamp et al. 1995) suggests that life history traits largely fall into two

categories—those with clear latitudinal and altitudinal trends (e.g., smolt outmigration and

spawn timing) and those without apparent trends (e.g., adult size and smolt size).

Presumably, traits with strong latitudinal/altitudinal trends are most affected by factors that

also have strong latitudinal trends (e.g., temperature, photoperiod), while traits that do not

show strong latitudinal trends may be affected by single factors without latitudinal trends or

by numerous factors working at smaller geographic scales.

One life history trait that shows a mixed pattern is freshwater age. Two species, pink

(O. gorbuscha) and chum (O. keta) salmon, always leave fresh water shortly after emergence.

In contrast, all other species examined (chinook (O. tshawytscha), sockeye (O. nerka), coho

(O. kisutch), Atlantic (Salmo salar), and masu (O. masou) salmon and steelhead (O. mykiss))

generally have extended (> or = 1 year) freshwater residence and clear latitudinal/altitudinal

trends in the duration of the residence.1

1 Both ocean-type chinook and sea-type sockeye salmon leave fresh water within their first

year, but only after spending several months in fresh water (Healey 1983, Wood 1995).
28

The difference in patterns of freshwater age (leaving immediately vs. extended

residence) suggests the existence of two general juvenile strategies used to make the

transition between fresh water and salt water. Possible advantages of the pink/chum (and, to a

lesser degree, ocean-type chinook and sea-type sockeye salmon) strategy include avoiding

fresh water and its associated problems (such as relatively low average productivity and high

mortality and low growth during winter), and taking advantage of highly productive estuarine

or nearshore marine habitats, where rapid growth can be achieved to quickly outgrow high

levels of size-specific predation. The other strategy (extended freshwater residence) might be

driven by low predation levels in freshwater habitats or a longer period of freshwater growth

to avoid high predation on small fish in estuarine and marine environments. Because fish

using these two strategies enter estuarine and marine waters at dramatically different ages

and sizes, they have different requirements from initial estuarine and marine habitats, and

mortality patterns are likely to be quite different. Consequently, the results of studies

examining populations using one type of strategy may not be relevant to populations using

the other strategy.

One example of how knowledge of freshwater residency may provide insight into

ocean mortality comes from freshwater age measurements from southeast Alaska populations

of coho salmon (Halupka et al. 1993), a species with extended freshwater residence.

Freshwater ages in these populations were measured on outmigrating smolts as well as

returning adults, allowing a comparison of freshwater age of fish going to sea with those

returning from sea. Although freshwater ages measured at these two stages were similar for

most populations, two populations were notable exceptions. In both cases, the average

freshwater age measured from the smolts was older than the freshwater age measured from

the adults, suggesting that ocean mortality within these populations was not random, but

rather was higher on the older juveniles. In this example, patterns of life history traits provide

insight about which fish do and do not survive, and suggest processes (i.e., low freshwater

growth rates) that might have some bearing on marine survival.

Another example of how life history traits provide insight into ocean residence comes

from ocean migration patterns for coho salmon as inferred from coded wire tag (CWT)

recovery patterns. We compiled marine (as defined in the database) CWT recovery records

(PSMFC 1994) for 65 coho salmon hatcheries from southeast Alaska to central California,

using recoveries expanded for sampling effort but not for untagged fish (Weitkamp et al.

1995). The proportion of recoveries occurring in each state or province for each hatchery are

indicated; CWT recovery patterns are fairly consistent among hatcheries within regions (e.g.,

British Columbia, Puget Sound and Hood Canal, Columbia River, etc.), but there are abrupt

changes between adjacent regions, rather than a gradual transition as might be expected due

strictly to the geographic location of the hatcheries (Fig. 1). For example, CWT recovery

patterns for coho salmon released from the Naselle Hatchery on Willapa Bay (Washington

coast) and from Grays River Hatchery on the lower Columbia River are very different from

each other, even though the two hatcheries are separated by less than 20 air miles. Naselle

and other Washington coast hatchery coho salmon have much higher recovery rates from

British Columbia and Washington and correspondingly lower recovery rates from Oregon
29

Figure 1. Marine recoveries by state or province of coded-wire-tagged coho salmon released

from selected hatcheries in Alaska (AK), British Columbia (BC), Washington

(WA), Oregon (OR), and California (CA). *Butte Falls Hatchery is located on the

Rogue River but rears Umpqua River coho salmon and releases them into the

Umpqua River (PSMFC 1994).
30

and California than do Grays River and other lower Columbia River hatchery fish (Fig. 1).

Although these patterns reflect only the last few months of a 1.5-year migration, the dramatic

differences in migration patterns suggest that there also may be significant differences earlier

in ocean residence as well.

Although patterns of CWT recoveries also vary over time, the responses of stocks

within a region are generally strongly correlated. Figure 2 displays the percentage of total

marine CWT recoveries from Oregon for fish released from Washington, Oregon, and

California coastal hatcheries between 1978 and 1992. Within each of the three regions,

patterns over time are very similar across populations, but they are quite different between

the three regions. This suggests that fish within each region are responding in similar manner

to the ocean conditions they encounter, but that conditions vary significantly between

regions.

We also examined trends in coho salmon adult size from different regions and found

the same pattern of high similarity within, and large differences between, regions,

particularly during anomalous years (Fig. 3). For example, Oregon coast coho salmon

returning to rivers north of Cape Blanco in 1983 were exceptionally small, presumably a

result of the strong El Niño that year (Johnson 1988). In contrast, coho salmon from rivers

south of Cape Blanco or north of the Columbia River were not unusually small in 1983,

suggesting they were not experiencing the same ocean conditions as the Oregon coast fish,

or, if they were, they were not affected to the same degree. Puget Sound coho salmon were

unusually small the following year (1984, Fig. 3), suggesting that either 1) conditions that

caused the small size for Oregon coast coho salmon also affected Puget Sound fish, but at an

earlier age, or 2) marine conditions moved and affected Puget Sound coho salmon at the

same age as the Oregon fish, but 1 year later.

The above discussion indicates that patterns for coho salmon ocean migration and

adult size exist at relatively small spatial scales. Other species or populations may show

patterns at different spatial scales. For example, Olsen and Richards (1994) compared trends

in abundance for stream-type chinook salmon from the Snake River with stream-type Fraser

River and ocean-type Puget Sound chinook salmon. Despite the much larger distance by

water between the Snake and Fraser River chinook salmon spawning grounds compared to

Snake River and Puget Sound spawning grounds, the former pair’s abundance trends were

very similar (r = 0.64), while those for the latter pair were not (r < or = 0.1). This suggests

that the factors that determine year class strength affected both Snake and Fraser River

populations in a similar fashion and were quite different than the factors that determine year

class strength for Puget Sound populations. The strength of the Fraser-Snake River

correlation, in spite of the presence of eight mainstem dams for the Snake River fish to

navigate and none for the Fraser River fish, suggests that ocean conditions play a key role in

overall mortality for stream-type chinook salmon in both systems. In this case,

geographically distant populations show more similarity than do geographically close

populations, which illustrates how life history trait patterns seem particularly useful at

indicating how widespread ocean processes and patterns might be.
31

Figure 2. Or-
32

Figure 3. Trends in adult size (weight [kg] of fish caught in in-river fisheries or length [mm

fork length] of natural spawners) for coho salmon populations from Puget Sound

and along the Washington and Oregon coasts, 1972-93.
33

A final example of how life history traits provide insight into estuarine and ocean

residence comes from the use of jack (precocious male) abundance as a predictor of the

following year’s adult abundance. Prior to 1983, Oregon coast and Columbia River coho

salmon jack (2 years old) abundance was a good predictor of adult (3 years old) abundance

(Pearcy 1992). Because jacks only spend 6 months at sea instead of 18 months for adults, this

suggested that much of the mortality that determined year-class strength occurred early in the

ocean residence. However, since 1983, the relationship between jack and adult abundance

has weakened, and jack abundance has been a poor predictor of adult run size in some years.

This change in the jack-adult relationship suggests two likely scenarios—either the timing of

significant mortality events has changed to later in the ocean residency, perhaps due to low

prey abundance, or the proportion of males that become jacks has become more variable, due

to large smolt size or poor ocean conditions in some years. Furthermore, Puget Sound coho

salmon jack run size has never been a good predictor of adult run size, suggesting a mortality

schedule quite different than that for Oregon coast coho salmon prior to 1983. In this

example, the relationship between jacks and adults provides information about when large

mortality events occur, indicates that these patterns can change over time, and shows how

widespread the patterns are.

To summarize, we have provided several examples of how life history trait

information provides valuable insight into patterns and processes that occur during estuarine

and ocean residency. These examples were the product of a fairly limited review of the

subject, and we expect that many more such examples will be unearthed with further

investigation. Although ocean residency is just one part of the salmon life cycle, considerable

insight about it can be gained by viewing it in the context of the larger life cycle.

Citations

Aro, K. V., and M. P. Shepard. 1967. Pacific salmon in Canada. Bull. Int. North Pac. Fish.

Comm. 23:225-327.

Atkinson, C. E., J. H. Rose, and T. O. Duncan. 1967. Pacific salmon in the United States.

Bull. Int. North Pac. Fish. Comm. 23:43-224.

Groot, C., and L. Margolis (editors). 1991. Pacific salmon life histories. Univ. British

Columbia Press, Vancouver, 564 p.

Halupka, K. C., J. K. Troyer, M. F. Wilson, and F. H. Everest. 1993. Identification of unique

and sensitive coho salmon stocks of southeast Alaska. Draft manuscript, U.S. Dep.

Agriculture, Pacific Northwest Research Station, Forest Sciences Laboratory, Juneau,

AK, 97 p. (Available from K. Halupka, Biology Dep., Albertson College of Idaho,

Caldwell, ID 83605.)
34

Healey, M. C. 1983. Coastwide distribution and ocean migrations patterns of stream- and

ocean-type chinook salmon, Oncorhynchus tshawytscha. Can. Field-Nat. 97:427-433.

Johnson, S. L. 1988. The effects of the 1983 El Niño on Oregon’s coho (Oncorhynchus

kisutch) and chinook (O. tshawytscha) salmon. Fish. Res. 6:105-123.

Olsen, D., and J. Richards. 1994. Inter-basin comparison study, Columbia River salmon

production compared to other West Coast production areas, Phase II analysis. Report

to the U.S. Army Corps of Engineers, 80 p. (Available from U.S. Army Corps of

Engineers, P.O. Box 2946, Portland, OR 97208-2946.)

Pacific States Marine Fisheries Commission (PSMFC). 1994. Regional Mark Information

System (RMIS) Coded-wire tag on-line database. (Available from Pacific States

Marine Fisheries Commission, 45 SE 82nd Dr., Suite 1000, Gladstone, OR 97027.)

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Washington Sea Grant

Program. Univ. Washington Press, Seattle, 179 p.

Weitkamp, L. A., T. C. Wainwright, G. J. Bryant, G. B. Milner, D. J. Teel, R. G. Kope, and

R. S. Waples. 1995. Status review of coho salmon from Washington, Oregon, and

California. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-NWFSC-24, 258 p.

Wood, C. C. 1995. Life history variation and population structure in sockeye salmon. In J. L.

Nielsen (editor), Evolution and the aquatic ecosystem: Defining unique units in

population conservation. Am. Fish. Soc. Symposium 17, Bethesda, MD, p. 195-216.
35

FACTORS INFLUENCING FRESHWATER AND MARINE SURVIVAL OF

OREGON’S COASTAL COHO SALMON—WHAT WE KNOW AND WHAT WE

DON’T

Steve Johnson

Oregon Department of Fish and Wildlife

Research and Development Section

Newport, OR 97365

In this paper, I review some of the factors that determine freshwater survival of coho

salmon (Oncorhynchus kisutch) in Oregon coastal streams and discuss ongoing research that

is evaluating how the quality of rearing habitat affects survival rates in fresh water. I also

review marine survival rates for Oregon coastal coho salmon and discuss an experiment

completed in the 1980s to determine if marine survival rates of hatchery reared coho salmon

could be increased by releasing them in various locations in the ocean off the Oregon and

Washington coasts.

In Oregon and throughout the Pacific Northwest, the freshwater life history of wild

coho salmon has been studied extensively (Bustard and Narver 1975a,b; Moring and Lantz

1975; Peterson 1982a,b; Hartman and Brown 1987; Nickelson et al. 1992). Wild coho

salmon in Oregon coastal rivers typically spawn in December and January in small tributary

streams. Their offspring emerge from the gravels the following spring and rear throughout

the summer and winter. In their second spring, the juveniles undergo physiological changes

that prepare them for the marine environment. Migration out of the upper tributaries begins in

March and April, and most fish enter the ocean by late May. Precocial males (jacks) return to

the coastal rivers the same autumn, while adults return after spending a year and a half at sea.

Past studies in the Pacific Northwest suggest average freshwater survival rates (egg to

smolt) of 2-3% throughout the region (Marshall and Britton 1990, Bradford 1995).

Researchers have long recognized the influence in spawner density on the freshwater survival

of coho salmon (Fig. 1). Recent research in Oregon coastal streams indicates the quality of

freshwater habitat also influences freshwater survival rates significantly, particularly during

the winter rearing period (Fig. 2).

Oregon has completed extensive aquatic habitat inventories in most Oregon coastal

watersheds since the late 1980s. We have combined this data set with our understanding of

the habitat quality/coho smolt production relationship developed from research streams to

estimate freshwater survival potential for many of our coastal river basins. These physical

habitat inventories indicate that habitat qualities, and therefore coho salmon freshwater

survival rates, vary significantly between watersheds, and are generally lower than previously

assumed (T. E. Nickelson, Oreg. Dep. Fish Wildl., 850 SW 15th St., Corvallis, OR 97333,

Pers. commun., March 1996).
36

Figure 1. The influence of spawner density on freshwater survival (egg to smolt) of juvenile

coho salmon in Deer Creek (Alsea River, Oregon). Data from Chapman (1965).

Figure 2. The relationship between juvenile coho salmon over winter survival and habitat

quality in Oregon coastal streams. Data from unpublished studies being conducted

by the Research Section of the Oregon Department of Fish and Wildlife.
37

We have few direct measurements of ocean survival for Oregon’s wild coho salmon,

but ocean survival of coho salmon reared and released from most Oregon coastal hatcheries

has dropped significantly during the last decade (Fig. 3) (Nickelson et al. 1994). Oregon

coastal hatcheries north of Cape Blanco have averaged only 1.6% ocean survival over the

past 10 years. These declines in marine survival have been correlated with various ocean

parameters, including upwelling and nearshore temperatures (Fig. 4) (Nickelson 1986, Fisher

and Pearcy 1988). While wild coho salmon stocks in Oregon may be surviving at two or

three times the rate of hatchery stocks, some wild stocks will have trouble replacing

themselves under present habitat conditions. Recent surveys of spawning adult coho salmon

indicate that this is indeed the case for some Oregon coastal basins.

Ocean conditions appear to have negatively affected coho salmon survival of most

Oregon coastal coho salmon stocks, particularly north of Cape Blanco. However, data from

adult spawning surveys completed every winter on Oregon’s central coast suggest that

estuaries may also sometimes play an important role in determining adult survival. In the past

2 years, we have observed significant differences in the number of recruits per spawner in

three central coast river basins (Siletz, Yaquina, and Alsea Rivers). The 1991 and 1992

broods from the Yaquina River showed a significant increase in spawners compared to the

number of parental spawners (apparently in response to a substantial decrease in ocean

harvest rate during 1994 and 1995). The Siletz and the Alsea Rivers (located approximately

30 km to the north and 18 km to the south of the Yaquina River, respectively) showed no

improvement in adult returns for the 1991 and 1992 broods (Fig. 5). Such different return

rates from river basins in such close geographic proximity suggest factors other than offshore

ocean conditions may be influencing smolt survival. Differential smolt survival within

estuaries would certainly produce the results recently observed in these three river basins and

needs to be considered as an additional factor that may play an important role in adult

production of Oregon’s wild coho salmon stocks.

To determine if marine survival could be influenced by release location in the marine

environment, experimental groups of hatchery reared coho salmon smolts were released into

the lower Columbia River (below Bonneville Dam at RKm 234), the Columbia River

estuary, and four marine locations off the mouth of the Columbia River from 1983 to 1987

(Solazzi et al. 1991). We chose release sites based on different oceanic features associated

with the mouth of the Columbia River and its discharge into the Pacific Ocean. The marine

release locations included 1) the mouth of the Columbia River, 2) the Columbia River plume

water, 3) coastal water approximately 19 km north and 19 km offshore of the mouth of the

river, and 4) oceanic water approximately 38 km offshore. Coho salmon smolts released at

the upper end of saltwater intrusion into the Columbia River (Rkm 29) survived at

significantly higher rates than fish released in fresh water below Bonneville Dam (Rkm 234).

The coho salmon smolts released directly into the ocean at the four marine release sites did

not survive at rates significantly different from those of the control groups released in fresh

water near Bonneville Dam, and they yielded few clues to the location or source of most of

the marine mortality. All groups showed interannual variation. Groups released in 1983

showed the poorest survival, resulting from the high ocean temperatures associated with the

El Niño event that year (Johnson 1988). Groups released in 1985 experienced the lowest
38

Figure 3. Marine survival of coho salmon smolts released from Fall Creek Hatchery (Alsea

River, Oregon), 1970-94.

Figure 4. The influence of ocean temperature and coastal upwelling on marine survival of

coho salmon released from Oregon hatcheries.
39

Figure 5. The recruits/spawner of coho salmon returning to three rivers on the central coast

of Oregon. Data from yearly spawning surveys conducted by the Oregon Department of Fish and Wildlife.
40

ocean temperatures during the spring, and all groups survived at their highest rate that year

(Table 1).

Citations

Bradford, M. J. 1995. Comparison of Pacific salmon survival rates. Can. J. Fish. Aquat. Sci.

52:1327-1338.

Bustard, D. R., and D. W. Narver. 1975a. Aspects of the winter ecology of juvenile coho

salmon (Oncorhynchus kisutch) and steelhead trout (Salmo gairdneri). J. Fish. Res.

Board Can. 32:667-680.

Bustard, D. R., and D. W. Narver. 1975b. Preferences of juvenile coho salmon

(Oncorhynchus kisutch) and cutthroat trout (Salmo clarki) relative to simulated

alteration of winter habitat. J. Fish. Res. Board Can. 32:681-687.

Chapman, D. W. 1965. Net production of juvenile coho salmon in three Oregon streams.

Trans. Am. Fish. Soc. 94:40-52.

Fisher, J. P., and W. G. Pearcy. 1988. Growth of juvenile coho salmon (Oncorhynchus

kisutch) in the ocean off Oregon and Washington, USA, in years of different coastal

upwelling. Can. J. Fish. Aquat. Sci. 45:1036-1044.

Hartman, G. F., and T. G. Brown. 1987. Use of small, temporary, floodplain tributaries by

juvenile salmonids in a west coast rain-forest drainage basin, Carnation Creek, British

Columbia. Can. J. Fish. Aquat. Sci. 44:262-270.

Johnson, S. L. 1988. The effect of the 1983 El Niño on Oregon’s coho (Oncorhynchus

kisutch) and chinook (O. tshawytscha) salmon. Fish. Res. (Amst.) 6:105-123.

Marshall, D. E., and E. W. Britton. 1990. Carrying capacity of coho salmon streams. Can.

Manuscript Rep. Fish. Aquat. Sci. 2058:1-32.

Moring, J. R., and R. L. Lantz. 1975. The Alsea watershed study; effects of logging three

headwater streams of the Alsea River, Oregon, Part I. Biological studies. Oreg. Dep.

Fish Wildl. Res. Rep. 9:1-39.

Nickelson, T. E. 1986. Influences of upwelling, ocean temperature, and smolt abundance on

marine survival of coho salmon (Oncorhynchus kisutch) in the Oregon production

area. Can. J. Fish. Aquat. Sci. 43:527-535.

Nickelson, T. E., J. Nicholas, H. Weeks, and K. Kostow. 1994. Oregon coho salmon

biological status assessment. Oreg. Dep. Fish Wildl., Corvallis, OR, 59 p.
41

Table 1. The number of adult coho salmon caught in ocean fisheries that were originally

released as smolts from various locations in the ocean, the Columbia River estuary,

and in the Columbia river 234 km upstream. The number of adult returns has been

adjusted to reflect a 40,000 smolt release for each group. See Solazzi et al. (1991)

for additional information.
42

Nickelson, T. E., J. D. Rodgers, S. L. Johnson, and M. F. Solazzi. 1992. Seasonal changes in

habitat use by juvenile coho salmon (Oncorhynchus kisutch) in Oregon coastal

streams. Can. J. Fish. Aquat. Sci. 49:783-789.

Peterson, N. P. 1982a. Population characteristics of juvenile coho salmon (Oncorhynchus

kisutch) overwintering in riverine ponds. Can. J. Fish. Aquat. Sci. 39:1303-1307.

Peterson, N. P. 1982b. Immigration of juvenile coho salmon (Oncorhynchus kisutch) into

riverine ponds. Can. J. Fish. Aquat. Sci. 39:1308-1310.

Solazzi, M. F., T. E. Nickelson, and S. L. Johnson. 1991. Survival, contribution, and return of

hatchery coho salmon (Oncorhynchus kisutch) released into freshwater, estuarine, and

marine environments. Can. J. Fish. Aquat. Sci. 48:248-253.
43

DECADAL SCALE CLIMATE PATTERN AND SALMON SURVIVAL

INDICATORS, INTERACTIONS, AND IMPLICATIONS

James J. Anderson

School of Fisheries

Box 358218

University of Washington

Seattle WA 98195-7980

Over this century, management strategies have been unsuccessful in halting the

salmon decline in the Columbia River system. Through the failures, an understanding of the

processes affecting the fishery has evolved an ecosystem perspective in which both

anthropogenic and natural factors are considered. In this paper, I illustrate how this history

has evolved using a stock-recruitment model that represents the assumptions and projections

through three management periods, each one an adaptive management experiment with

unique problems and a management paradigm. In recent years, this cycle has been coined

adaptive management, where learning is achieved through management actions (Lee 1993).

Adaptive management involves a number of basic steps outlined in Figure 1. An

action taken on a resource is based on a prior prediction of its effect. The actual effect is

monitored, either by exploitation of the resource or through a specific monitoring program,

and the results are evaluated through comparison with the prior prediction. Discrepancies

between the predicted and observed effects are used to modify the management paradigm and

develop new actions and predictions.

Model

To illustrate how the management paradigm can change between experiments,

consider a Ricker-type stock-recruitment model that contains mortality associated with

hydrosystem passage, harvest, habitat loss, and changes in ocean/climate conditions. The

model assumes a generic chinook salmon (Oncorhynchus tschawytscha) stock with a fixed

maturation at age 4. For each cohort, the model first removes harvest; second, generates

recruits, and third, updates the population. The algorithm is

Si = S.preharvest - harvest*S.preharvesti

Ri = f*habitati*Si * exp (-passagei - climatei- b*Si )

S.preharvest(i + 1) = Si

 + Ri

where for generation i, S.preharvesti is the harvestable population, Si is the population with

harvest removed, Ri is recruitment, habitati is a measure of spawning habitat, f is egg

production per adult, passagei is hydrosystem mortality, climatei

 is mortality attributed to

climate-induced changes in survival, b is a density dependent mortality rate, and harvesti is
44

Figure 1. Steps in an adaptive management experiment.

Figure 2. The history of the Columbia River has three major adaptive management

experiments: harvest, hydrosystem development, and fishery rebuilding.
45

the harvest rate. These factors are set to represent the beliefs during each management period

or experiment. Factors not accounted for in an experiment are held constant.

Important trends in the Columbia River history, representing basic paradigm shifts,

fall into three adaptive management experiments: 1) harvest experiment (1866-1932),

2) hydro development experiment (1932-75), and 3) fishery rebuilding experiment (1975-95).

The periods are illustrated with chinook salmon harvest, hydro development, and hatchery

output in Figure 2.

Adaptive Management Experiments

The harvest experiment began with the Columbia River commercial fisheries (1860)

and ended with the construction of the first mainstem dam (1932). The industry quickly

expanded and stabilized between 1890 and 1920. In addition to harvest, salmon production

was affected by a cumulative loss of habitat due to farming, grazing, timber harvest,

irrigation, and mining (Lichatowich and Mobrand 1995). These losses were largely ignored

and unregulated. Ocean and climate effects were unknown.

During the harvest experiment, managers assumed that overharvest was the major

reason for the catch decline and the solution was to regulate fishing. The stock recruitment

model illustrates that, assuming all other factors were constant, harvest reductions should

have stabilized the fishery (Fig. 3). Since catch was relatively stable between 1890 and 1920,

there was no compelling reason to believe that limited harvest restrictions were not effective.

The decline accelerated after 1920, which motivated the banning of stationary fishing gear in

1934.

A hydrosystem development experiment followed between 1932 and 1975 when 19

major dams were built on the Columbia and Snake Rivers and many more were built in the

tributaries. It was clear that the dams destroyed spawning habitat and degraded river passage.

To deal with adult upstream passage, fish ladders were installed on the mainstem dams below

Chief Joseph and Hells Canyon Dams, but the problem of juvenile downstream passage was

not addressed. To replace lost habitat, hatcheries were constructed; by 1975 the biomass of

hatchery smolts released into the Columbia River Basin equaled the adult catch (5 million

pounds) (Fig. 2). Expressing these assumptions in the model, catch would have increased by

about 1950, and a significant reduction in the harvest rate would not be required (Fig. 4).

Mitigation through hatcheries and fish ladders was unsuccessful, so a third cycle of

adaptive management, the stock rebuilding experiment, commenced with a program

including monitoring, evaluation, and models. The focus was in four areas: harvest, habitat,

passage, and fish production. In particular, smolt migration was identified as a problem and

actions were taken to improve downstream passage survival. These included a water budget

to speed smolt migration, juvenile bypass facilities and spill to divert smolts from turbines,

and a program to collect and transport Snake River smolts to below Bonneville Dam. In
46

Figure 3. The harvest experiment strategy was to limit harvest rate.

Figure 4. Management actions in the hydro development experiment included adult passage

ladders and replacing lost habitat with hatcheries.
47

addition, since gains made in smolt passage could be lost in harvest, additional fishing

regulations were implemented. With the rebuilding program assumptions represented in

Figure 5, the stock decline should have been halted in the 1980s.

These management actions did not stop the decline which has again brought managers to

question the underlying assumptions on which the actions were based. As a result, the

research/management community is moving into a fourth adaptive management experiment,

the focus of which is to understand the fisheries through an ecosystem approach. In

particular, the new focus examines the effect of decadal scale climatic and oceanic variation

on fish survival. Earlier management paradigms ignored this factor.

To represent the effect of climate and ocean conditions, consider the Pacific Northwest Index

(PNI), which consists of air temperature, rainfall, and snowpack data from the Northwest

(Ebbesmeyer and Strickland 1995). The PNI pattern is similar to other climate indicators

which show relationships to fish abundance and catch over the North Pacific (Beamish

1995). Of particular importance, all the climate indicators have a pronounced shift in 1976-77

when the North Pacific changed from a cool regime to a warm regime. The cool regime was

favorable to West Coast salmon stocks and the warm regime was favorable to Alaskan

stocks.

To illustrate the potential impact of climate, the stock recruitment model assumes the PNI is

directly related to the salmon ocean survival rate (Fig. 6). During hydrosystem development

the PNI was high, while during the stock rebuilding phase the PNI was low. If ocean survival

followed the same trend, the negative impact of the hydrosystem during its development

would be masked by the concomitant favorable ocean conditions. Also, the large replacement

of lost habitat with hatcheries postulated in earlier management experiments (Figs. 4 and 5) is

not required. Otherwise the stocks would have significantly increased during the rebuilding

experiment.

The 1975-76 ocean regime shift, producing unfavorable conditions for fish, complicates the

interpretation of the effectiveness of hatchery actions. Coronado-Hernandez (1995), in an

analysis of salmonid hatchery survivals from the West Coast and Alaska, concluded that

ocean conditions were partially responsible for the decline in hatchery productivity while

disease and genetic changes were not significant factors. Previously, declining hatchery

productivity was generally attributed to such factors.

The ocean regime shift also complicates the interpretation of efforts to improve smolt

passage after 1976. Of particular importance is the transportation program. One hypothesis,

which ignores the ocean effect, attributes the Snake River wild chinook salmon decline to

fish transportation. The evidence offered is a correspondence in the decline of survival

expressed as a smolt-to-adult ratio (SAR) (U.S. Department of Commerce 1995) to the

percent of Snake River fish that were transported. Figure 7 suggests that survival went down

when transportation increased.
48

Figure 5. The fishery rebuilding experiment involved new actions including harvest

restrictions and improved juvenile passage. The model indicates the stock would

improve beginning about 1980.

Figure 6. The ecosystem adaptive management experiment includes climate factors and

downgrading of the effectiveness of habitat actions.
49

Figure 7. Snake River spring chinook salmon smolt-to-adult survival and percent of the run

transported.

Figure 8. Pacific Northwest Index (PNI) climate indicator and juvenile passage survival

estimate (S) move in opposite directions and result in declining smolt-to-adult

survival (SAR).
50

An alternative hypothesis assumes that in-river survival has improved and fish

transportation has been effective (survival of transported fish greater than 80%), but passage

survival improvements were negated by poor ocean conditions. This hypothesis is supported

by studies indicating high smolt survival through the Snake River (Muir et al. 1996), and

estimates generated from the CRiSP1.5 mainstem passage model (Anderson et al. 1996),

which show improving smolt passage survival since the early 1970s. The improvement is

attributed to reduced gas bubble disease, improved dam operations (Williams and Matthews

1995), and the transportation program which was initiated in 1977. The contention that

climate change negated passage improvements is supported in Figure 8 which shows a

negative correlation between the PNI climate index and CRiSP estimated in-river survival

between 1966 and 1990. Furthermore, prior to 1975, the smolt-to-adult survival followed the

CRiSP in-river survival pattern, suggesting that the poor passage conditions during the

construction of the lower Snake River dams was a significant factor in lowering smolt-toadult survival between 1966 and 1975. After 1975, the SAR followed the PNI, which

switched to the regime unfavorable to West Coast salmon. This suggests that poor ocean

survival was a major contributor to the low SAR after 1975.

Conclusions

Climate clearly has had an impact on the decline of Columbia River salmon and

compels a reinterpretation of the anthropogenic impacts, principally harvest and the

hydrosystem. The significance of climate is suggested in the patterns of the PNI, the

hydrosystem generating capacity, and Columbia River chinook salmon catch (Fig. 9). Three

features are noteworthy: 1) the catch decline in 1920 corresponds with PNI change from a

cool/wet regime to a warm/dry regime; 2) hydrosystem development, starting in the 1940s,

was concomitant with the PNI switching back to the cool/wet regime; 3) the stock rebuilding

effort, beginning in 1976, occurred with the PNI returning to the warm/dry regime.

The start of the catch decline in 1920 is possibly the result of a change in climate

conditions and an inability of the harvest restrictions at the time to fully compensate for the

environmental change (compare Figs. 3 and 6). The fact that the catch decline did not steepen

during the hydrosystem development is likely the result of a return to favorable ocean

conditions which compensated for the adverse effects of the dams (compare Figs. 4 and 6),

and the failure of the stocks to increase with the rebuilding efforts in the 1980s (compare

Figs. 5 and 6) was likely in part the result of unfavorable ocean conditions, which have

counteracted improvements in smolt passage survival.

This revised interpretation for the Columbia River stock decline may never be fully

supported, because of the lack of long-term historical data on fish survival. In any case, it is

clear that the coincidence of major natural and anthropogenic events did occur and that the

fishery decline cannot be explained by anthropogenic factors alone. Realizing that natural

and anthropogenic processes interact over decadal scales, the community of Columbia River

scientists and managers has embarked on a new ecosystem perspective for managing the
51

Figure 9. Major reversals in the Pacific Northwest Index (PNI) were concomitant with the

beginning of Columbia River chinook salmon harvest decline (1), the initiation of

hydropower development (2), and the beginning of the salmonid transportation

program (3).
52

resource. The current focus is on the effects of climate, but an expanding ecosystem

perspective, including such factors as fish physiology, behavior, and genetics, will lead to a

more realistic understanding of the limitations and opportunities available to improve the

Columbia River.

Summary

The influence of decadal scale climatic variations on the decline of Columbia River salmon

was not realized until recently. I evaluated the implications of this omission using a stock

recruitment model with climatic and anthropogenic factors. I concluded that fisheries

managers over the past century have misinterpreted the anthropogenic impacts on Columbia

River salmon. In particular, I suggest three major events have been misinterpreted:

1) managers overestimated the significance of harvest on the catch decline after 1920 by not

accounting for climatic changes that lowered ocean survival at this time, 2) managers

underrepresented the detrimental effects of the hydrosystem by not accounting for the

contribution of good ocean survival during the years of hydrosystem development and,

3) managers underestimated the success of stock rebuilding measures in the last two decades

because the concomitant poor ocean survival was not accounted for. I also suggest that the

fisheries community is now evolving an ecosystem approach that considers both

environmental and anthropogenic impacts on salmon.

Citations

Anderson, J., J. Hayes, P. Shaw, and R. Zabel. 1996. Columbia River salmon passage model

(CRiSP.1.5), 220 p. University of Washington, School of Fisheries, WH-10, Seattle,

WA 98195.

Beamish, R. J. 1995. Climate change and northern fish populations. Can. Spec. Publ. Fish.

Aquat. Sci. 121:739 p.

Coronado-Hernandez, M. C. 1995. Spatial and temporal factors affecting survival of

hatchery-reared chinook, coho and steelhead in the Pacific Northwest. Ph.D. Thesis,

University of Washington, Seattle, 235 p.

Ebbesmeyer, C. C., and R. M. Strickland. 1995. Oyster condition and climate: Evidencefrom

Willapa Bay. Washington Sea Grant Program, Univ. Washington, Seattle, Publ.

WSG-MR 95-02, 11 p.

Lee, K. N. 1993. Compass and gyroscope: Integrating science and politics for the

environment. Island Press, Washington, DC, 243 p.
53

Lichatowich, J. A., and L. E. Morbrand. 1995. Analysis of chinook salmon in the Columbia

River from an ecosystem perspective. Report to Bonneville Power Administration,

Contract DE-AM79-92BP25105, 102 p. (Available from Bonneville Power

Adminstration, Public Information Center-CKPS-1, P. O. Box 3621, Portland, OR

97208.)

Muir, W. D., S. G. Smith, E. E. Hockersmith, S. Achord, R. F. Absolon, P. A. Ocker, B. M.

Eppard, T. E. Ruehle, J. G. Williams, R. N. Iwamoto, and J. R. Skalski. 1996.

Survival estimates for the passage of yearling chinook salmon and steelhead through

Snake River dams and reservoirs, 1995. Report to U.S. Army Corps of Engineers,

Contract E86940119, and Bonneville Power Administration, Contract DE-A179-

93BP10891, 150 p.

U.S. Department of Commerce, National Oceanic and Atmospheric Administration,

1995.Proposed recovery plan for Snake River salmon, 490 p. (Available from

Environmental and Technical Services Division, National Marine Fisheries Service,

525 NE Oregon Street, Suite 500, Portland, OR 97232-2737.)

Williams, J. G., and G. M. Matthews. 1995. A review of flow and survival relationshipsfor

spring and summer chinook salmon, Oncorhynchus tschawytscha, from the Snake

River Basin. Fish. Bull., U.S. 93:732-740.
54
55

Interannual Variations in Northeast Pacific Marine

Habitats and the Effects on Marine Survival of Salmonids
56
57

COASTAL OCEAN CIRCULATION OFF OREGON: RECENT OBSERVATIONS OF

SPATIAL AND TEMPORAL VARIABILITY

Jack A. Barth and Robert L. Smith

College of Oceanic and Atmospheric Sciences

Oregon State University

104 Ocean Admin. Bldg

Corvallis, OR 97331-5503

Ocean circulation off the northwest coast of the United States is driven by a variety of

mechanisms, the most important of which is the seasonally varying wind stress. The response

of the coastal ocean to strong equatorward (“upwelling-favorable”) winds during the summer,

described for example off the Oregon coast based on a number of past studies (e.g., Huyer

1983), consists of net offshore transport in the surface Ekman layer, upwelling of cold, saline

water near the coast, and the formation of a strong alongshore coastal jet that is in

geostrophic balance with the upwarped isopycnals. Winds become predominantly upwellingfavorable after the “spring transition” (Huyer et al. 1979), and the upwelling regime persists

through the summer and early fall before returning to winter conditions after a fall transition.

During the upwelling regime, the vertical structure of the alongshore velocity field consists

of a southward coastal jet in the upper water column extending down to 50-75 m depth, with

maximum speeds near the surface of up to 1 knot, and a more sluggish poleward undercurrent

near the bottom over the outer continental shelf (Huyer et al. 1978).

The summer upwelling circulation is affected on short time scales by changes in the

wind stress on 2- to 10-day time scales (Huyer 1983). On longer time scales, the timing and

intensity of the upwelling circulation varies from year to year (Huyer et al. 1979, Strub and

James 1988) under the influence of interannual variability in the atmospheric driving and in

coupled ocean-atmosphere phenomena, for example El Niño (Huyer and Smith 1985). The

following discussion will not focus on interannual variability of coastal ocean circulation,

except to point out differences between two particular years along the Oregon coast (1994

and 1995), concentrating instead on a description of spatial variation of the upwelling

circulation associated with the interaction of a strong upwelling jet with a coastal

promontory. Spatial variability in the coastal upwelling circulation is readily apparent in

satellite sea surface temperature (SST) maps, an example of which is shown in Figure 1.

Spatial variability is an important factor to consider, together with temporal variability, when

assessing the influence of the coastal ocean on biological productivity and the transport of

biogeochemical and anthropogenic material.
58

Figure 1. Top: Vector winds (m/s) for 1994 measured at the NOAA CMAN station in

Newport, Oregon. The date of the sea surface temperature image is denoted by a

gray bar. Bottom: Satellite infrared sea surface temperature (°C) from 18 August

1994 showing cold, upwelled water near the coast separated from warmer water

offshore by a meandering front.
59

The Coastal Jet Separation Experiment

Recently, scientists at Oregon State University (OSU) have been studying the region

near Cape Blanco, Oregon in an effort to understand how and why the strong alongshore

coastal upwelling jet turns offshore, crosses the steep topography of the continental margin,

and becomes an oceanic jet (Barth et al. 1994, Barth and Smith 1996, Smith et al. 1996). The

Cape Blanco region was chosen because historical observations (Huyer 1990, Smith 1992)

and satellite imagery (Fig. 1) suggest that this is a dividing point between a region to the

north of the cape where upwelling is fairly well confined to inshore of the continental shelf

break (approximately the 200-m isobath) and a region to the south of the cape where a

meandering equatorward jet and upwelled water extend well seaward of the continental

margin (Kosro and Huyer 1986).

The observational component of the Coastal Jet Separation Experiment consisted of

three hydrographic and velocity surveys during 1994 and 1995 using the Research Vessel

(RV) Wecoma, tracking surface drifters and analyzing satellite SST imagery. The

hydrographic data were collected using a towed, undulating vehicle, SeaSoar (Pollard 1986),

which cycles rapidly from the surface to depth while towed at 8 knots (4 m/s) behind the RV

Wecoma. The majority of the conductivity-temperature-depth data was collected by towing

the SeaSoar on a bare cable cycling the vehicle between 0 and 120 m every 4 minutes. The

result is hydrographic data with very high spatial resolution (1 km between along-track

surface points) obtained rapidly (cross-shelf sections in 2-3 hours and large-area maps in 1-2

days) so that a detailed “snapshot” of the system can be studied. Over the shallow continental

shelf, the SeaSoar was flown from 0 to 55 m cycling every 1.5 minutes, resulting in alongtrack profile spacing as little as one-third of a kilometer. The SeaSoar was also towed

occasionally on a cable equipped with aerodynamic fairing to reduce drag; this allows the

vehicle to cycle between the surface and in excess of 300 m every 8 minutes.

The seasonal cycle in the wind stress is apparent in the 1994 winds as measured at

Newport, Oregon (Fig. 1, top). July was a month of typical, strong upwelling-favorable

winds; however, August was a period of anomalously weak equatorward winds. An SST

image from 18 August 1994 (Fig. 1, bottom) reveals a band of cold upwelled water near the

coast, confined to inshore from the continental shelf break north of Cape Blanco (the wide

cold feature near lat. 44°N is the influence of Heceta Bank—note the bottom topography in

Fig. 3) and extending much farther seaward south of the Cape. The equatorward upwelling

jet, associated with the temperature front between cold upwelled water inshore and warmer

water offshore, meanders westward at Cape Blanco but returns toward the coast downstream

in a counter-clockwise bend before meandering over 300 km offshore near lat. 41°N. A ship

survey of the region on 25 to 30 August 1994 (Fig. 2) confirmed the existence of the strong

alongshore coastal jet north of the Cape as exemplified by the strong gradient in dynamic

height found there. Geostrophic currents flow along contours of dynamic height, and their

speed is inversely proportional to the distance between the contours. The dynamic height

map shows continuity of the southward jet with a counter-clockwise (cyclonic) eddy roughly

80 km in diameter offshore from the Cape. A second dynamic height map reveals the
60

Figure 2. Contour maps of dynamic height normalized by the acceleration of gravity

(∆D23/55/g in meters) from SeaSoar surveys during 25-30 August 1994 (left) and 29

August to 2 September 1994 (right). Individual conductivity-temperature-depth

profiles are denoted by dots along the ship track and the 0.9-m dynamic height

contour is highlighted to emphasize the pinching off of a counter-clockwise

(cyclonic) eddy off Cape Blanco, Oregon.
61

Figure 3. Trajectories of three satellite-tracked drifters released on 25 August 1994 at the

beginning of the SeaSoar surveys shown in Figure 2. Release points off Coos Bay

are denoted by asterisks; marks along the drifter tracks are at weekly intervals.

Trajectories are shown from the release until 18 October 1994 (left), where the

most landward drifter (long dashed line) failed on 5 September 1994, and for the

remaining two drifters through 27 March 1995 (right), where the drifter denoted by

the solid line reached lat. 49°N on 26 December 1994.
62

pinching off of the eddy and a reconnection of the equatorward jet on the inshore side, as

denoted by the 0.9-m dynamic height contour. This creation of a large counter-clockwise

eddy is termed “cyclogenesis” and is a result of a flow-topography interaction between the

coastal upwelling jet and the Cape. The eddy contains water of coastal origin, and this

process is an important mechanism for injecting biologically important material into the deep

ocean.

Three satellite-tracked surface drifters were released across the coastal jet to the north

of Cape Blanco (Fig. 3) at the beginning of the survey. All three drifters were initially swept

offshore by the separating jet, but the most inshore drifter (long dashed curve) split from the

other two to follow an inshore pathway to the south (compare with the 0.8-m dynamic height

contour in Fig. 2). The other two drifters moved together around the northern edge of the

cyclonic eddy at speeds of up to 0.6 m/s, before one drifter (dashed curve) moved off to the

northwest while the other drifter made one complete revolution of the eddy before exiting to

the north. Both drifters then made counter-clockwise revolutions around a cold eddy (near

lat. 43°N, long. 126.5°W in the SST image) formed earlier (July) in the upwelling season.

One drifter (dashed curve) again left the cyclonic feature to the north and spent the next 5

weeks in the low velocity region well offshore from central Oregon, while the other drifter

remained trapped in the counter-clockwise eddy. In mid-October, the winds became southsouthwesterly through the fall transition (Fig. 1) and the circulation responded as shown by

drifter tracks in the right-hand panel of Figure 3. The drifter in the stagnant offshore area was

swept back onto the continental shelf, returning very close to its deployment point after

spending 2.5 months offshore. This demonstrated a Lagrangian pathway for passive particles

to leave the coastal ocean, but to then return through the influence of seasonally and spatially

varying circulation. The other drifter executed additional revolutions around the eddy before

also being swept onto the central Oregon shelf. Since the cold offshore eddy was formed in

July, this indicated a minimum eddy lifetime of 4-5 months. Finally, both drifters were swept

rapidly poleward by the Davidson Current (Jones 1918) transiting to north of Vancouver

Island.

In 1995, winds became upwelling-favorable for an extended period beginning in midMay (Fig. 4, top). A satellite SST image from 18 May 1995 (Fig. 4, bottom) showed a

relatively narrow band of cold, upwelled water near the coast during this early part of the

upwelling season. The southward-upwelling jet and front meandered only slightly near Cape

Blanco (compare the SST image in Fig. 1). A ship survey of the Cape Blanco region (not

shown) confirmed the existence of the nearly straight southward jet near the continental shelf

break. Five satellite-tracked surface drifters were released across the continental margin north

of Cape Blanco on 21 May 1995 (Fig. 5, left). The four inshore drifters transited rapidly to

the south at speeds up to 0.6 m/s, again demonstrating the relatively straight alongshore flow

(compare with Fig. 3, left). The drifter released farthest west was placed in the surface

salinity minimum associated with the Columbia River influence offshore from the coastal

upwelling jet and front, and transited slowly (0.05-0.25 m/s) to the southwest. Throughout

the remainder of the upwelling season, the drifters were swept equatorward in the eastern

boundary current region by a meandering jet (Fig. 5, right). Evidence for eddies, meanders,
63

Figure 4. Top: Vector winds (m/s) for 1995 measured at the NOAA CMAN station in

Newport, Oregon. The date of the sea surface temperature image is indicated by an

arrow and the times of two R/V Wecoma cruises are denoted by gray bars.

Bottom: Satellite infrared sea surface temperature (°C) from 18 May 1995 showing

a relatively narrow band of cold, upwelled water near the coast at the beginning of

the upwelling season.
64

Figure 5. Trajectories of five satellite-tracked drifters released on 21 May 1995 off Coos

Bay, Oregon. Drifter tracks are shown for 1 week (left) and for 8 1/2 months

(right) after the release. For the early trajectories, drifter tracks are all drawn as

solid curves while in the right-hand panel tracks are differentiated by line type.

The drifter released second-farthest west failed on 30 May 1995. An additional

drifter (thin dashed curve) is included in the right-hand panel beginning on 31 May

1995 just to the north of the earlier five-drifter release latitude.
65

swift jets, and more sluggish flow far offshore (e.g., near lat. 37-40°N, long. 129-132°W)

exists in the drifter tracks. These Lagrangian trajectories confirm the hypothesis that the

separating coastal upwelling jet off Oregon contributes significantly to the meandering jet

now accepted as making up a large fraction of the equatorward flow in the California Current

System (Huyer et al. 1991). None of the drifters released in May returned to the coast, nor did

they remain or return to their release latitude. This demonstrates that material carried by the

coastal upwelling jet off Oregon early in the upwelling season can be carried far from its

point of origin by the swift, relatively linear southward flow.

A ship survey and drifter release was conducted near the end of August 1995 after a

period of typical strong upwelling-favorable wind stress (Fig. 4, top). A map of dynamic

height (Fig. 6, left) shows a strong southward jet centered on the continental shelf break north

of Cape Blanco which then meandered offshore near the Cape and separated from the coast

to become an oceanic jet. The jet gained in strength downstream from the Cape, in part from

a flow contribution that joined the separating jet from the northwest (lat. 43.25°N, long.

125.5°W) and was associated with flow around Heceta Bank upstream. Five satellite-tracked

drifters were released on the continental shelf north of Cape Blanco (Fig. 6, right) and

initially all were carried to the south in the upwelling jet. While the most inshore drifter

grounded south of Cape Blanco, the other four drifters were swept swiftly (speeds in excess

of 1 m/s) offshore in the separating jet. The drifters executed both clockwise (anticyclonic)

and cyclonic loops associated with the strong, unstable meandering jet. Drifters released on

the shelf transit over 400 km from the coast before turning southward and delineating the

equatorward eastern boundary current jet with its core located between long. 127°W and

128°W near lat. 40°N. As the winds become south-southwesterly in the fall, the circulation

responds, and all four drifters were swept shoreward between lat. 37°N and 39°N. By 7

February 1996, one drifter (thin dashed curve) had come ashore south of Cape Mendocino,

another drifter (thick solid curve) was transiting poleward over the continental slope, one

drifter (thin solid curve) had exited from a cyclonic eddy near lat. 38°N, long. 127°W and

was transiting shoreward to the northwest, and the fourth drifter (thick dashed curve) stopped

transmitting over the continental slope just north of Point Arena. In summary, as a result of

the jet-topography interaction which leads to a meandering jet with a substantial east-west

component, passive material released on the shelf in the coastal upwelling jet north of Cape

Blanco, Oregon can return to the coast within approximately 5 degrees of latitude to the

south under the influence of the seasonal change in wind stress and the resulting ocean

circulation.

Discussion

The results presented here demonstrate the existence of strong spatial variability in

the upwelling circulation off the Oregon and northern California coasts. Understanding the

processes which lead to and control this spatial variability is critical in assessing the

influence of ocean circulation on biological productivity and the transport of biogeochemical

and anthropogenic material onto and off of the continental shelf. The existence of separated

coastal upwelling jets, recirculating eddies, meandering equatorward jets, and return flows to
66

Figure 6. Left: Contour map of dynamic height normalized by the acceleration of gravity

(∆D23/55/g in meters) from a SeaSoar survey during 19-23 August 1995. Individual

conductivity-temperature-depth profiles are denoted by dots along the dynamic

height contour is highlighted to show the separation of the coastal jet from the

continental shelf. Right: Trajectories of five satellite-tracked drifters released on

19 August 1995 off Coos Bay, Oregon. The drifter released farthest north and

most landward (thick solid curve) ran aground just south of Cape Blanco on 15

September 1995, one drifter (thin solid curve) failed on 28 November 1995 just

offshore of the 2000-m isobath north of Pt. Arena, and one drifter (thin dashed

curve) came ashore south of Cape Mendocino on 16 December 1995.
67

the coast has been documented. There is a distinct difference in the behavior of the system

early (May) versus later (August) in the upwelling season. In May, the coastal jet remains

relatively straight as it transits around Cape Blanco, and drifters released on the shelf are

flushed far to the south in the eastern boundary current region. This differs from the behavior

later in the upwelling season (August) when the upwelling circulation is more fully

developed and the jet-topography interaction creates a spatially complex flow pattern that can

retain drifters released on the shelf near their release latitude, enabling their return to the

continental margin after the seasonal winds change direction.

Finally, interannual changes in the strength and timing of upwelling occur and are

important to levels of biological productivity. While this paper has not concentrated on

interannual variability, marked differences exist between the two August realizations

presented here. In August 1994, upwelling-favorable winds were anomalously weak and the

jet-cape interaction resulted in the generation of cyclonic eddies. In August 1995, after a

month of typical strong upwelling-favorable winds, the coastal jet was fully separated from

the coast near Cape Blanco. To better understand interannual variability, both further

understanding of dynamic processes (which lead to strong spatial variability) and long time

series of oceanographic and atmospheric conditions are needed.

Acknowledgments

We are indebted to Jane Huyer (OSU) for her encouragement during this research and

for her insights on coastal and eastern boundary current circulation. Thanks also to the OSU

Marine Technicians, Marc Willis, Tim Holt, Linda Fayler, and Mike Hill, who were

responsible for the highly successful SeaSoar operations. The officers and crew of the

RV Wecoma performed superbly—only occasionally would they comment on the fact that

we insisted on towing the SeaSoar in an east-west direction, invariably in the trough of the

prevailing northwest summer swell. Ted Strub and Corinne James (OSU) generously

provided the satellite imagery. This work was funded by National Science Foundation Grant

OCE-9314370.

Citations

Barth, J. A., and R. L. Smith. 1996. Separation of a coastal upwelling jet and pathways for

cross-shelf exchange: A Lagrangian perspective. Eos Trans. AGU, Ocean Sciences

Meet. Suppl. 77(3):130.

Barth, J. A., R. L. Smith, and A. Huyer. 1994. Separation of a coastal jet and cyclogenesis

during coastal upwelling. Eos Trans. AGU, Fall Meet. Suppl. 75(44):345.
68

Huyer, A. 1983. Coastal upwelling in the California Current system. Prog. Oceanogr. 12:259-

284.

Huyer, A. 1990. Shelf circulation. In B. LeMehaute and D. M. Hanes (editors), Ocean

engineering science (The Sea, Vol. 9, Pt. A), p. 423-466. Wiley, New York.

Huyer, A., P. M. Kosro, J. Fleischbein, S. R. Ramp, T. Stanton, L. Washburn, F. P. Chavez,

T. J. Cowles, S. D. Pierce, and R. L. Smith. 1991. Currents and water masses of the

coastal transition zone off northern California, June to August 1988. J. Geophys. Res.

96:14809-14831.

Huyer, A., and R. L. Smith. 1985. The signature of El Niño off Oregon, 1982-83. J. Geophys.

Res. 90:7133-7142.

Huyer, A., R. L. Smith, and E. J. C. Sobey. 1978. Seasonal differences in low-frequency

current fluctuations over the Oregon continental shelf. J. Geophys. Res. 83:5077-

5089.

Huyer, A., E. J. C. Sobey, and R. L. Smith. 1979. The spring transition in currents over the

Oregon continental shelf. J. Geophys. Res. 84:6995-7011.

Jones, E. L. 1918. The neglected waters of the Pacific Coast. Spec. Publ. U.S. Coast Geodetic

Survey 48:1-21.

Kosro, P. M., and A. Huyer. 1986. CTD and velocity surveys of seaward jets off northern

California, July 1981 and 1982. J. Geophys. Res. 91:7680-7690.

Pollard, R. 1986. Frontal surveys with a towed profiling conductivity/temperature/depth

measurement package (SeaSoar). Nature 323:433-435.

Smith, R. L. 1992. Coastal upwelling in the modern ocean. In C. P. Summerhayes, W. L.

Prell, and K-C. Emeis (editors), Upwelling systems: Evolution since the early

Miocene, p. 9-28. Geological Soc. London Spec. Publ. 64.

Smith, R. L., J. A. Barth, and A. van Geen. 1996. The coastal upwelling jet: A link between

coastal upwelling and the California Current. Eos Trans. AGU, Ocean Sciences Meet.

Suppl. 77(3):130.

Strub, P. T., and C. James. 1988. Atmospheric conditions during the spring and fall

transitions in the coastal ocean off the western United States. J. Geophys. Res.

93:15561-15584.
69

THE FOOD ENVIRONMENT OF JUVENILE SALMONIDS:

YEAR-TO-YEAR VARIATIONS IN ZOOPLANKTON ABUNDANCE

OVER THE INNER-MIDDLE SHELF OFF CENTRAL OREGON—1969-78

William T. Peterson

NOAA/NMFS Hatfield Science Center

2030 Marine Science Dr.

Newport, OR 97365

A number of statistical studies have demonstrated that the survival of coho salmon

(Oncorhynchus kisutch) in the ocean is correlated positively with the strength of coastal

upwelling (Fig. 1) during the summer of smolt out-migration (first noted by Gunsolus in

1978; reviewed in Pearcy 1992). The causal variable(s) which might account for the positive

correlations are not known; in papers that discuss such correlations, it is often stated that

summers having good upwelling represent “good ocean conditions” and summers having low

upwelling represent “poor ocean conditions.” The purpose of this paper is to attempt to

improve the definition of the term “ocean conditions,” using as a proxy the abundance of

zooplankton over the continental shelf.

Methods

As an index of ocean conditions, two kinds of data are presented, the Bakun

upwelling index and the speed and direction of winds measured at the Newport, OR South

Jetty. The wind data are presented as progressive vector diagrams; data shown here have

been published (Peterson and Miller 1975, 1976).

The biological data are from a series of zooplankton samples collected from June

1969 through 1972, and another series of samples collected during late-spring and summer of

1973, July/August 1977, and July/August 1978. The 1969-72 samples were collected as part

of a survey of copepods and ichthyoplankton carried out by Sally Richardson, Bill Pearcy,

and Charles Miller with the aid of Oregon Sea Grant funding. Results of this project have

been published (e.g., Richardson and Pearcy 1977; Peterson and Miller, 1975, 1977). Most of

the zooplankton samples were collected with a 20-cm bongo net fitted with 240-μm-mesh

plankton nets; zooplankton were enumerated by species and developmental stage. A

summary of all data from 1969 to 1972 is published in a technical report (Peterson and Miller

1976).

The zooplankton data are presented in two ways. First, data for all years for a given

species are pooled in a series of illustrations that show the seasonal cycle of abundance.

Second, the data are broken out by abundance, by year, and for July/August (since these are

the months for which the most data are available).
70
71

Results

Wind Data

Upwelling-favorable winds (i.e., winds which blow southward) usually begin to blow

in mid-April and continue through early September off central Oregon. The winds are never

continuous from north to south; rather the pattern is punctuated by periods of either calm

winds or reversals during which winds may blow from the south and east. The intermittency

of the winds generates what are known as upwelling events. Figure 2 shows an example of

each of the two patterns usually observed off central Oregon in summer. During 1969, 1970,

and 1973, the winds were predominantly from the north with very little onshore set to the

wind. During the summers of 1971 and 1972, there was a greater preponderance of winds

from the east. The wind data from all 5 years may be summarized as follows:

 Thousands of

wind-kilometers Number Bakun upwelling index, 45°N

Year S E of events (summed weekly values; May-August)

1969 14 2 7 675

1970 22 1 9 782

1971 9 12 8 574

1972 38 15 11 624

1973 14 6.5 6 712

Read this table as follows: for 1969, if you multiplied wind speed by vector of direction, you

would find that the wind “blew” a total of 14,000 km toward the south (i.e., from the north)

and 2,000 km toward the east (i.e., from the west), from May through August. A comparison

of south to east winds among years shows that winds were more easterly in 1971 and more

southerly in the other years. The Bakun upwelling index is fairly well correlated with the

southerly wind for all years but 1972.

Zooplankton (Copepods)

Highest zooplankton abundances are found within the upper 20 m of the water

column over the inner- and mid-shelf (Peterson and Miller 1975, 1976). The dominant

species are copepods and they are found in distinct ecological zones, parallel to the coast. A

near-shore group is made up of Acartia clausii, Centropages abdominalis, and

Pseudocalanus mimus. The offshore group is composed of Acartia longiremis and Oithona

similis. The life history stages of Calanus marshallae are distributed across both zones, with

eggs and nauplii near shore and older juveniles farther from shore. Relationships between

zonation of copepod species, hydrography, and mechanisms for population retention are

discussed in Peterson et al. (1979).
72

Figure 2. A progressive vector diagram of the winds at South Jetty, Newport, Oregon, for

two contrasting years: 1970 and 1971.
73

The seasonal cycle of abundance is shown in Peterson and Miller (1977). Here, I

show the climatological cycle (i.e., all data are pooled regardless of year) for 1969-73 and for

1978 for the dominant species. Considering first the small copepods (<1.5 mm length and

<30 μ g dry weight), the two species of Acartia have a common abundance pattern (Fig. 3);

both populations begin to increase in numbers in early June; A. clausii reaches peak

abundances in October, whereas A. longiremis peaks as early as mid-July. The main growth

period for the copepods Pseudocalanus mimus and Centropages abdominalis is also JuneOctober, with peak abundances in July. For the large copepod Calanus marshallae (adult

length 3.5 mm and dry weight 350 μ g), the population begins to increase in mid-February

(Fig. 4). High numbers of adults can be seen throughout the spring and summer months.

Zooplankton (Euphausiids)

Euphausiids are one of the chief prey of juvenile coho salmon (Peterson et al. 1982;

Emmett et al. 1986; Brodeur 1989; Brodeur and Pearcy 1990, 1992). Though one does not

sample the adults and older juveniles quantitatively with small bongo nets, one can learn

something of the distribution and abundance of adults by the presence or absence of eggs and

larval stages. Based on the egg data shown in Figure 5, adults begin spawning in mid-April

and continue to do so through the summer. Apart from the nauplii which showed a strong

peak in summer, the other life-cycle stages are about equally abundant in spring as in

summer. The presence of high numbers of eggs from May through August suggests that adult

euphausiids are abundant throughout this period.

Relationships between zooplankton and juvenile coho salmon

The copepod data can be summarized in terms of total copepod biomass. Biomass

was calculated by multiplying copepod numbers by weights of individuals. The table below

summarizes these data along with abundances for euphausiid furcilia (juveniles) for data

collected in July/August since those are the months for which the most data are available.

These data can be compared to percent coho salmon survival:

 Small-

 copepod Calanus Euphausiid Coho

 biomass biomass numbers survival

(mg m-3) (mg m-3) (m-3) (%)

1969 187 38 79 7.5

1970 70 10 35 9.0

1971 43 10 51 4.5

1972 25 4 68 4.1

1973 99 7 171 7.8

1977 — 98 — 4.2

1978 85 32 0 3.0
74
75

Figure 4. Seasonal cycle of abundance of Calanus marshallae males, females, and juveniles.

This species overwinters in the autumn, from October (Day 275) until the first of

the year. The population begins to increase in February, reaching a peak in early

September (approx. Day 250).
76
77

The coho salmon survival data can be sorted into “good” years (1969, 1970, and

1973) and “bad” years (1971, 1972, 1977, and 1978). Using total biomass of small copepods,

biomass of Calanus, or numbers of euphausiids as indicators of ocean conditions, I conclude

that 1969, 1977, and 1978 were good years for zooplankton and 1971 and 1972 were poor

years. There is poor agreement between these two sets of years, so no conclusions concerning

relationships between zooplankton biomass and coho survival can be reached. Also, linear

regression between copepod biomass, Calanus biomass, or euphausiid numbers (in July/

August) and coho salmon survival were not significant. Thus it is unclear how upwelling is

related to ocean conditions with respect to coho salmon survival (in terms of using

zooplankton abundance or biomass as a proxy for ocean conditions). However, a problem

with this analysis is that coho salmon survival and zooplankton in July/August were

compared. If coho salmon survival is established during the first few weeks they are at sea,

then ocean conditions during the peak of the upwelling season (July/August) may be

unimportant. Perhaps our attention should focus on the April/May period.

Juvenile coho salmon enter the coastal ocean in April/May. This migration is not

related to the seasonal cycle of copepod abundance since the seasonal peaks in abundance of

the dominant (but small) copepods (Acartia, Pseudocalanus, and Centropages) occur in July

and August. Not surprisingly, these small copepods are not prey for juvenile coho. The coho

migration may be timed to the seasonal cycles of abundance of their major prey items. For

their fish prey, sand eel (Ammodytes) larvae are most abundant in March/April (Richardson

and Pearcy 1977), implying that juvenile sand eels are abundant in April/May, and smelt

(osmeriid) larvae peak in May/June, with juveniles abundant in June/July. For the larger

zooplankton, the observation that euphausiid spawning commences in mid-April implies that

adults are present in the water column and are available to juvenile salmonids. Also, the

largest copepod which is common off the Oregon coast in spring, Calanus marshallae, is

abundant during this April/May window. Thus I suggest that salmon migrations may be

timed to the presence or abundance of their preferred prey. If we are to find meaningful

correlations between prey abundance and salmon survival, direct measurements may be

required of the abundance of their preferred prey in April and May.

There may, however, be a proxy variable that can serve as a correlate. I hypothesize

that the oceanographic feature that is driving food-chain dynamics in April/May (and that

may be related to salmon mortality) is the timing of the onset of upwelling, the so-called

“spring transition.” This event is correlated with the appearance of euphausiids in continental

shelf waters off central California (D. G. Ainley, Point Reyes Bird Observatory, 4990

Shoreline Highway 1, Stinsom Beach, CA 94970. Pers. commun., 1996), for example, and

may be related to a redistribution of fish prey off Oregon since coastal circulation patterns

change as upwelling is initiated. If the coho salmon migration is fixed in time, but the spring

transition is variable, perhaps a classical “match-mismatch” set of events is important here.

For example, if the spring transition is initiated later in the spring (e.g., in May) at the present

time as compared to during the 1960s and 1970s, the coho salmon may be arriving at sea

sooner than the time of greatest availability of their prey. Thus they may be encountering
78

“poor ocean conditions” in April that are not related to strength of upwelling, but to the

timing of the onset of the upwelling season.

Conclusions

There were no clear relationships between zooplankton abundance and coho salmon

survival. This was due chiefly to the fact that the peak abundance of zooplankton occurred in

July/August, several months after juvenile coho salmon enter the sea. Future work on

possible relations between food availability and coho salmon survival must include intense

sampling in the April-May period, and must target their chief prey—sand eels, smelt,

euphausiids, and larger copepods. We did learn from the study of seasonal cycles of

zooplankton, that euphausiids begin to spawn in mid-April, at the time of the spring

transition. Since coho salmon arrive at sea at the same time, I suggest that future

retrospective analyses of coho salmon and ocean conditions should look for correlations

between data of spring transition and coho salmon survival. Moreover, work on relationships

between date of spring transition, the possible movement of euphausiids onto the shelf, and

the possible redistribution of juvenile fish prey (sand eels and smolt) at this time might

provide a partial answer to the question of what is meant by the phrase “good vs. poor ocean

conditions” with respect to coho salmon.

Citations

Brodeur, R. D. 1989. Neustonic feeding by juvenile salmonids in coastal waters of the

Northeast Pacific. Can. J. Zool. 67:1995-2007.

Brodeur, R. D., and W. G. Pearcy. 1990. Trophic relations of juvenile Pacific salmon off the

Oregon and Washington coast. Fish. Bull., U.S. 88:617-636.

Brodeur, R. D., and W. G. Pearcy. 1992. Effects of environmental variability on trophic

interactions and food web structure in a pelagic upwelling ecosystem. Mar. Ecol.

Prog. Ser. 84:101-119.

Emmett, R. L., D. R. Miller, and T. H. Blahm. 1986. Food of juvenile chinook,

Oncorhynchus tshawytscha, and coho, O. kisutch, salmon off the northern Oregon and

southern Washington coasts, May-September 1980. California Fish Game 72(1):38-

46.

Gunsolus, R. T. 1978. The status of Oregon coho and recommendations for managing the

production, harvest and escapement of wild and hatchery-reared stocks. Oregon Dep.

Fish. Wildl. Processed Rep., 59 p. (Available from Oregon Dept. Fish. Wildl., P.O.

Box 59, Portland, OR 97207.)
79

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Univ. Washington Press,

Seattle, 179 p.

Peterson, W. T., R. D. Brodeur, and W. G. Pearcy. 1982. Food habits of juvenile salmon in

the Oregon coastal zone, June 1979. Fish. Bull., U.S. 80:841-851.

Peterson, W. T., and C. B. Miller. 1975. Year-to-year variations in the planktology of the

Oregon upwelling zone. Fish. Bull., U.S. 73:642-653.

Peterson, W., and C. Miller. 1976. Zooplankton along the continental shelf off Newport,

Oregon, 1969-1972: Distribution, abundance, seasonal cycle and year-to-year

variations. Oregon Sea Grant Program, Oregon State Univ., Publ. ORESU-T-76-002,

111 p.

Peterson, W. T., and C. B. Miller. 1977. Seasonal cycle of zooplankton abundance and

species composition along the central Oregon coast. Fish. Bull., U.S. 75:717-724.

Peterson, W. T., C. B. Miller, and A. Hutchinson. 1979. Zonation and maintenance of

copepod populations in the Oregon upwelling zone. Deep-Sea Res. 26A:467-494.

Richardson, S. L., and W. G. Pearcy. 1977. Coastal and oceanic fish larvae in an area of

upwelling off Yaquina Bay, Oregon. Fish. Bull., U.S. 75:125-145.
80
81

INTERANNUAL VARIABILITY IN GROWTH AND SURVIVAL

OF CHINOOK AND COHO SALMON

Peter W. Lawson

Oregon Department of Fish and Wildlife

2040 SE Marine Science Drive

Newport, OR 97365

Spring upwelling in the year of ocean entry is generally recognized as an oceanic

indicator of coho salmon (Oncorhynchus kisutch) recruitment (Nickelson 1986, Pearcy 1992,

Lawson 1993). Recent discussions (this conference) have focused on the observation that, in

the Oregon Production Index (OPI) area, south of Leadbetter Point, Washington, hatchery

coho salmon smolt-to-adult survival has not been correlated with upwelling in the current

period of low upwelling years. Nickelson (1986) showed that in all low upwelling years

between 1960 and 1981 there had been no correlation between hatchery survival and

upwelling. I suggest that upwelling, by itself, is not an adequate indicator of ocean

conditions. Winter sea surface temperature in the adult return year is independent of

upwelling and, in combination with upwelling, can be used to explain much of the variation

in recruitment of naturally spawning coho salmon in Oregon. Survival and recruitment of

hatchery coho salmon, primarily from the Columbia River, are affected by freshwater factors

including variability in rearing and release practices and problems with disease. These fish

enter an ocean more heavily influenced by the Columbia River freshwater plume and less

strongly affected by upwelling compared with the more southerly distributed Oregon coastal

natural (OCN) stocks. For these reasons, it is likely that OCN and hatchery stock groups

would respond differently to changes in ocean conditions. Recruitment time series, rather

than survival, are used for analysis because there are no direct estimates for naturally

produced smolts from Oregon over the period from 1970 to 1996.

Table 1 presents a 25-year time series of ocean population size (adult recruits to the

fishery) for public hatchery and OCN coho salmon, along with spring upwelling (UW) at lat.

42°N (Bakun 1975) and winter sea surface temperature (SST) anomalies at Charleston,

Oregon. Note that the OCN recruit estimates are an index which is thought to overestimate

true abundances by about 50% to 80% (Jacobs and Cooney 1994). Although the numerical

estimates are biased high, they capture the interannual variations in recruitment which are the

subject of this analysis. The UW, SST, and hatchery and OCN recruits time series show

significant correlations with year, indicating secular trends (Table 2). The signs on all trends

are negative except for SST, which has been increasing. Upwelling and SST are strongly

correlated with OCN recruits (P < or = 0.0005), less strongly with hatchery recruits (0.07 > P

> 0.002), but not with each other (P > 0.38, Table 2). The lack of a significant correlation

between UW and SST is unusual in ocean environmental time series and supports their use as

indicators of two independent oceanic processes. Autocorrelation within time series implies

that the effective number of degrees of freedom is less than the number of years in the series
82

Table 1. Oregon public hatchery and coastal natural coho (OCN) salmon ocean recruitment,

with two environmental variables. Recruitment in thousands of fish. Sea surface

temperature (SST) anomaly; deviation from mean 1971-95 January + February sea

surface temperature at Charleston, Oregon, °C, upwelling (UW) anomaly; deviation

from mean April + May + June Bakun upwelling index, lat. 42°N.
83

Table 2. Pearson correlation coefficinets (P < > 0) of Oregon public hatchery and Oregon

coastal natural (OCN) coho salmon recruitment and two environmental variables.

See also Table 1.
84

(Kope and Botsford 1990). Employing the conservative correction described by Kope and

Botsford (1990), the correlation between OCN recruits and SST remains significant

(P < 0.02), and OCN recruits with UW is marginally significant (0.10 > P > 0.05).

Together, UW and SST explain most of the variability in OCN coho salmon

recruitment since 1970, including years affected by El Niño. Multiple linear regression of the

natural log of recruits vs. UW and SST explains about 75% of the variability in recruitment

(Figs. 1 and 2; Table 3, Model 1). Although there is a secular trend in all three time series

(Table 2), the residuals from the regression still show a secular decline. Accounting for this

decline would explain an additional 16% of the variation. Upwelling and SST explain only

about 27% of the variability in hatchery coho salmon recruitment, with UW not a significant

factor in the regression (Table 3, Model 2).

Several factors may contribute to an apparent lack of correlation between upwelling

and hatchery coho salmon recruitment (or survival) in recent years. Figure 2 compares OCN

and hatchery coho recruits plotted against an index of ocean conditions calculated from the

model parameters presented in Table 3, Model 1. The index is 0.011*UW - 0.365*SST.

Average ocean conditions from 1971 to 1995 receive an index of zero. All but 2 years since

1984 show below-average ocean conditions. Although recent years have shown low

recruitments for OCN coho salmon, the overall pattern of increasing recruitment with

improved ocean conditions is consistent across the full range of ocean conditions. Hatchery

coho salmon, on the other hand, show much more variable recruitment when plotted against

this index. Years prior to 1984 fit the general pattern of higher recruitment with favorable

ocean conditions. However, recent years show no pattern. Considerable experimentation with

hatchery rearing and release practices has been conducted in the past 15 years, complicating

interpretation of these data. Winter SST seems to be much more important than UW in

explaining variability in public hatchery recruitment (Tables 2 and 3, Model 2). Spring SST

in the year of ocean entry has been identified as having high correlation with hatchery

survival (T. E. Nickelson, Oregon Dep. Fish Wildl., 850 SW 15th St., Corvallis, OR 97333.

Pers. commun., 1996).

Time series of average weights from ocean commercial troll fishery landings, and a

condition factor based on a regression of weight vs. length, show interannual variations that

may provide insights into life history processes not evident from the recruit data. Chinook

salmon average weights since 1950 show a decadal fluctuation, with higher weights in the

1950s and 1970s (Fig. 3a). In contrast, coho salmon show a decline in average weight since

1950 (Fig. 3b). Both species tended to be small in size during the strong El Niños in 1957-58

and 1982-83. Scale analysis of OCN coho salmon shows no evidence of a decline in size

between 1950 and 1990, so this trend may be specific to hatchery reared coho salmon (D.

Bottom, Oregon Dep. Fish Wildl., 850 SW 15th St., Corvallis, OR 97333. Pers. commun.,

1996.). Weight:length functions (Fig. 4) for coho salmon suggest both environmental and

density-dependent factors may be operating. In years with relatively normal ocean conditions

(1984, 1985, and 1986), the length:weight regressions have similar slopes. Fish were shorter

and in poorer condition in 1986, when ocean populations of coho salmon in the waters off
85

Figure 1. Modeled response surface and observed Oregon coastal natural (OCN) coho

salmon recruitment, 1971-95. Model: Recruits = 5.06 ÷ 0.011*Upwelling -

0.37*SST, adjusted r2 - 0.75.
86

Figure 2. Ocean recruitment of Oregon coastal natural (OCN) and public hatchery origin

coho salmon from 1971-95, plotted against an index of ocean conditions calculated

from the regression of sea surface temperature and upwelling on OCN coho salmon

recruits. Recruit numbers in thousands. Open circles: 1971-83; closed circles:

1984-95.
87

Table 3. Regression statistics. See also Table 1.
88

Figure 3. Average weights of chinook (a) and coho (b) salmon in the commercial troll

salmon fishery off newport, Oregon, in July from 1952-91. Weights are for trolldressed fish (gutted, head on).
89

Figure 4. Length: weight relationship of coho salmon landed in Newport, Oregon, for 5

years. Heavy lines indicate years affected by El Niño. Length of line reflects

range of observations.
90

Oregon were over three times as abundant as in either 1984 or 1985, indicating that growth

rates may have been reduced at high ocean densities. The 2 years of strong El Niño show the

highest contrast. While mean lengths and weights were identical, and the range of sizes was

similar, the slopes of the regressions diverged. In 1983, longer fish were of lower weight,

while in 1992 it was the shorter fish that were low in weight. The 1982-83 El Niño was

unusual, with effects reaching the Oregon coast by October 1982, compared with the 1992

event, which reached Oregon in January 1992. The length:weight function in 1992, with low

abundance and poor ocean conditions, was remarkably similar to 1986, with high abundance

and better ocean conditions.

Mechanisms linking UW and SST with survival and growth of coho salmon in

Oregon are not well known. Pearcy (1992) presents a recent review of salmonid ocean

ecology, with emphasis on coho salmon. Brodeur and Pearcy (1990) and Fisher and Pearcy

(1990) investigated early oceanic life history of coho and chinook salmon from 1981 to 1985.

Aside from these studies, little has been done to investigate mechanisms of survival in the

ocean. Upwelling in the year of ocean entry affects the nearshore oceanic environment by

increasing production, lowering temperatures, and adding spatial complexity in the form of

fronts and thermal breaks (J. Barth and Smith, this volume). It may also affect the

movements of predators and the availability of salmon smolts to predators. Winter SST is an

index of the quality of offshore oceanic conditions, which are affected by atmospheric

conditions in the central North Pacific (Norton and McLain 1994; Parrish, this volume). Sea

temperatures may affect predator movements, indicate nutrient regimes, or be linked to

bioenergetics of salmon and their prey. Other factors potentially contributing to trends in

OCN recruitment include declines in freshwater productivity (Lawson 1993), density

dependent survival (McGie 1984, Emlen et al. 1990), accumulated effects of hatchery coho

salmon interactions with wild fish, and a trend since 1970 of later onset of upwelling. Future

investigations should focus on discovering the links between indices of ocean conditions and

the ocean life history of Pacific salmonids.

Citations

Bakun, A. 1975. Daily and weekly upwelling indices, West Coast of North America, 1967-

73. U.S. Dep. Commer., NOAA Tech. Rep. NMFS SSRF-693. 114 p.

Brodeur, R. D., and W. G. Pearcy. 1990. Trophic relations of juvenile Pacific salmon off the

Oregon and Washington coast. Fish. Bull., U.S. 88:617-636.

Emlen, J. M., R. R. Reisenbichler, A. M. McGie, and T. E. Nickelson. 1990. Densitydependence at sea for coho salmon (Oncorhynchus kisutch). Can. J. Fish. Aquat. Sci.

47:1765-1772.
91

Fisher, J. P., and W. G. Pearcy. 1990. Spacing of scale circuli versus growth rate in young

coho salmon. Fish. Bull., U.S. 88:637-643.

Jacobs, S. E., and C. X. Cooney. 1994. Improvement of methods used to estimate the

spawning escapement of Oregon coastal natural coho salmon. Oreg. Dep. Fish Wildl.

Ann. Prog. Rep. 24 p.

Kope, R. G., and L. W. Botsford. 1990. Determination of factors affecting recruitment of

chinook salmon Oncorhynchus tshawytscha in central California. Fish. Bull., U.S.

88:257-269.

Lawson, P. W. 1993. Cycles in ocean productivity, trends in habitat quality, and the

restoration of salmon runs in Oregon. Fisheries (Bethesda) 18(8):6-10.

McGie, A. M. 1984. Commentary: Evidence for density dependence among coho salmon

stocks in the Oregon Production Index area. In W. G. Pearcy (editor), The influence

of ocean conditions on the production of salmonids in the North Pacific, p. 37-49.

Oregon State Univ. Sea Grant, Corvallis.

Nickelson, T. E. 1986. Influences of upwelling, ocean temperature, and smolt abundance on

marine survival of coho salmon (Oncorhynchus kisutch) in the Oregon Production

Area. Can. J. Fish. Aquat. Sci. 43:527-535.

Norton, J. G., and D. R. McLain. 1994. Diagnostic patterns of seasonal and interannual

temperature variation off the west coast of the United States: Local and remote largescale forcing. J. Geophys. Res. 99(8):16,019-16,030.

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Washington Sea Grant

Program, University of Washington Press, Seattle, 179 p.

2.08

1978 1607.3 371.4 1.304 17.08

1979 1157.5 641.4 -1.246 -2.92

1980 1059.2 348.2 0.554 17.08

1981 927.4 338.6 1.704 -1.92

1982 1199.7 314.9 -0.296 -8.92

1983 502.8 226.4 1.354 14.08

1984 646.9 274.2 0.504 -24.92

1985 656.6 303.2 -0.346 -24.92
92
93

Decadal Variations in Northeast Pacific Marine Habitats

and the Effects on Marine Survival of Salmonids
94
95

REGIME-SCALE FLUCTUATIONS IN THE CIRCULATION

OF THE NORTH PACIFIC

Richard H. Parrish

Pacific Fisheries Environmental Group

Southwest Fisheries Science Center

National Marine Fisheries Service

1352 Lighthouse Ave.

Pacific Grove, CA 93950

The first fisheries researcher to suggest that environmental changes were a controlling

factor in multidecade fluctuations of fish stocks was Ljungman (1880). In his paper

“Contribution Toward Solving the Question of the Secular Periodicity of the Great Herring

Fisheries,” Ljungman presented the known fluctuations of the Bohuslan herring fisheries

from the 19th century back to the 9th century and suggested that there was about a 55-year

periodicity in the abundance of herring. He further suggested that the fishery fluctuations

were caused by “periodical and secular changes in the direction and intensity of the currents

of the sea, by which a change in the occurrence of herring food and the consequent

migrations of the large schools of herring could be explained.”

There was little advancement in multidecadal-scale fisheries analyses for nearly a

century; then, a number of researchers on sardines and anchovies from several major current

systems came to a consensus that not only were major stocks of sardines and anchovies

fluctuating on a multidecadal or “regime” time scale, but there were obvious similarities in

the timing of regimes in widely separated current systems (Kawasaki and Omori 1988,

Lluch-Belda et al. 1989, Lluch-Belda et al. 1992). More recent work has shown that other

stocks were affected by the now well-known 1976 regime shift in the northeastern Pacific

(Beamish 1993, Beamish and Bouillon 1993).

In an attempt to determine oceanic features associated with the observed biological

regimes, I have used the Climate and Eastern Ocean Systems (CEOS) version of the

Comprehensive Ocean-Atmosphere Data Set (COADS) (Mendelssohn and Roy in press) to

develop time series and decadal difference maps for a variety of marine surface observations

in an attempt to describe recent regime shifts. The widespread changes associated with the

1976 regime shift are clearly seen in the differences in decadal sea-level atmospheric

pressures, surface winds, and sea-surface temperatures in the mid-latitude North Pacific.

Sea level pressure data show that the principal difference between the pre- and post1976 decades is an intensification and eastward expansion of the winter (DecemberFebruary) Aleutian low pressure system (Fig. 1). The pressure fields give the visual

impression that the major change was centered around lat. 48°-55°N. From an oceanographic

point of view this is misleading, since the principal oceanographic effect of the pressure field
96

Figure 1. Mean December-February sea level atmospheric pressure (mb) by 2 degrees of

latitude and longitude for the pre- and post-1976 decades.
97

is not associated with the position or intensity of the low but with the winds which are a

function of the gradient in atmospheric pressure.

In the decade prior to 1976, the region of maximum winter winds, as seen in fields of

eastward pseudostress (i.e., the means of the squares of the east component of the wind

observations), was centered at about lat. 40°N and long. 160°W (Fig. 2). In contrast, in the

period of 1977-86, there was a major increase in eastward pseudostress and the maxima were

displaced well to the southeast. Thus, the major change was not in the vicinity of the Aleutian

low pressure system but on the subtropical side of the West Wind Drift region.

The third major aspect of the regime shift is the change in sea surface temperature

(SST). In winter, the eastern North Pacific was between 0.5° and 1.5°C warmer in the post1976 decade than in the pre-1976 decade (Fig. 3). The Aleutian Islands and southern Bering

Sea also had warmer winter SST in the recent decade. In contrast, the majority of the central

North Pacific (i.e., lat. 20°-45°N and long. 150°E-150°W) was colder in the post-1976

decade. The maximum difference occurred in the Oyashio-Kuroshio mixing area, just west of

Northern Honshu where winter SST was between 1.5° and 2°C lower during 1977-86 than

during 1966-75. The winter pattern of colder SST suggests that much of the colder,

subtropical side of the North Pacific Current is moved southwards in the region to the east of

the dateline. In summer, the SST decadal difference pattern is somewhat different than in

winter, with the colder water region displaced to the east with an extension of colder water

almost to the coast off of Oregon and Washington. There is also an intensification and

expansion of the warmer SST region in the Alaska Stream region. The summer temperature

difference in the Oyashio-Kuroshio mixing area is considerably less than in winter.

While the sea level pressure and SST changes are relatively easy to visualize, the

physical effects of the wind changes are much more complex. Wind has a number of physical

effects on the sea, and these effects are different functions of the wind. For example,

turbulent mixing is a function of the cube of the wind speed and is independent of wind

direction, whereas Ekman transport is a function of the square of the wind vector. Divergence

and convergence patterns are a function of the gradient of the wind, and geostrophic transport

is a function of the wind curl or the divergence of Ekman transport. Thus, changes in the

wind field alter a wide range of factors, including sea surface temperature, the depth of the

upper mixed layer, upwelling, frontal formation, wind-driven currents and wind stress curldriven currents. Polovina et al. (1995) have shown that there was a major decadal shift in

winter and spring mixed layer depths and mixed layer temperatures in association with the

1976 regime shift. In particular, there was a sharp increase in mixed layer depth in a region

centered at about lat. 35°N and extending from about long. 155°E to about 155°W. The

geographical pattern of decadal differences in wind speed cubed, an index of turbulent

mixing, is very similar to this reported increase in mixed layer depth. The region of increased

mixed layer temperatures described by Polovina et al. (1995) is very similar to the area of

increased SST from the COADS data (Fig. 3).
98

Figure 2. Mean December-February eastward pseudostress (m/sec)2 by 2 degrees of latitude

and longitude for the pre- and post-1976 decades.
99

Figure 3. February and August sea surface temperature differences (degrees C) between the

pre- and post-1976 decades by 2 degrees of latitude and longitude.
100

Although there is a distinct difference in the environmental data fields from the two

decades, time series show that the regime shift occurred earlier in the northwestern Pacific

than in the northeastern Pacific. Winter sea surface temperatures from the Oyashio-Kuroshio

mixing region show that the shift occurred in this region in 1971, whereas the shift is

generally considered to have occurred in 1976-77 in the northeastern Pacific.

The principal force altering the oceanographic conditions associated with the 1976

regime shift in the northeastern Pacific appears to be the great increase in winter eastward

wind stress which was centered in the central and western North Pacific at about lat. 32-38°N

(Fig. 2). This alteration in the winter winds resulted in a significant change in the surface

wind-stress curl, which is the forcing function for the vertically integrated mass transport of

the North Pacific Current. Decadal averages of mid-North Pacific winter, eastward

pseudostress (averaged by 2° of latitude and 20° of longitude) suggest that the wind curldriven flow of the North Pacific Current was intensified and centered at a lower latitude in

the post-1976 decade (Fig. 4). In the pre-1976 decade, winter eastward pseudostress

increased between lat. 57°N and 47°N, with the region between 43°N and 35°N having

values near 40 (m/sec)2, and then decreased between 33°N and 21°N. In the post-1976

decade, eastward stress increased to a maximum of 85 (m/sec)2 at 35°N and decreased rapidly

between 33°N and 21°N. In contrast, there was little difference in the divergenceconvergence pattern during spring in the two decades (Fig. 5). The increase and equatorward

expansion of the winter divergence pattern in the post-1976 decade would result in a lower

latitude, more subtropical source for water entering the California and Alaska Currents; this,

in turn, represents the probable major cause of the anomalously warm SST which occurred in

both regions.

Citations

Beamish, R. J. 1993. Climate and exceptional fish production off the west coast of North

America. Can. J. Fish. Aquat. Sci. 50:2270-2291.

Beamish, R. J., and D. R. Bouillon. 1993. Pacific salmon production trends in relation to

climate. Can. J. Fish. Aquat. Sci. 50:1002-16.

Kawasaki,T., and M. Omori. 1988. Fluctuations in the three major sardine stocks in the

Pacific and the global trend in temperature. In T. Wyatt and M. G. Larreñeta (editors),

Long-term changes marine fish populations, p. 37-53. Instituto de Investigaciones

Marinas de Vigo, Vigo, Spain.

Ljungman, A. 1880. Contribution toward solving the question of the secular periodicity of

the great herring fisheries. Rep. U.S. Fish. Comm. 1879:497-503.
101

Figure 4. Winter (December-February) wind speed cubed differences (m/sec)3 between the

pre- and post-1976 decades by 2 degrees of latitude and longitude (1977-86 minus

1966-75).
102

Figure 5. Winter and spring east pseudostress (m/sec)2 at long. 160°W-180°W by 2 degrees

of latitude.
103

Lluch-Belda, D., R. J. M. Crawford, T. Kawasaki, A. D. MacCall, R. H. Parrish, R. A.

Schwartzlose, and P. E. Smith. 1989. World-wide fluctuations of sardine and anchovy

stocks: The regime problem. S. Afr. J. Mar. Sci. 8:195-205.

Lluch-Belda, D., R. A. Schwartzlose, R. Serra, R. Parrish, T. Kawasaki, D. Hedgecock, and

R. J. M. Crawford. 1992. Sardine and anchovy regime fluctuations of abundance in

four regions of the world oceans: A workshop report. Fish. Oceanogr. 1(4):339-347.

Mendelssohn, R., and C. Roy. In press. CODE (Comprehensive Ocean Data Extraction)

Users Guide. U.S. Dep. Commerc., NOAA-TM-NMFS-SWFSC-228.

Polovina, J. J., G. T. Mitchum, and G. T. Evans. 1995. Decadal and basin-scale variation in

mixed layer depth and the impact on biological production in the Central and North

Pacific, 1960-88. Deep-Sea Res. 41(10):1701-1716.
104
105

DECADAL-SCALE ENVIRONMENTAL VARIABILITY IN THE COASTAL

NORTHEASTERN PACIFIC

Franklin B. Schwing, Richard Parrish, and Roy Mendelssohn

Pacific Fisheries Environmental Group

1352 Lighthouse Avenue

Pacific Grove, CA 93950

The physical environment of the northeastern Pacific fluctuates substantially on a

number of seasonal and longer scales, some periodic and predictable, and some not obviously

so. El Niño Southern Oscillation (ENSO) events and other perturbations produce profound

anomalies in the atmosphere and ocean on interannual to decadal and century time scales.

This area also can be separated into discrete spatial regions, dominated by different physical

processes that are presumably collocated with unique biological structures. The timing and

intensity of large-scale climate events may not be coherent between regions. The boundaries

defining these regions may change over time as well. Our objective is to describe decadalscale differences in the spatial texture of the northeastern Pacific, to provide a base from

which to evaluate the effect of climate change on the area’s ecosystems, and particularly on

its salmonid populations and fisheries.

The data analyzed in this paper are summarized from the Comprehensive OceanAtmosphere Data Set (COADS). Monthly time series for 1946-90 were constructed from

COADS sea surface temperature (SST) and wind stress data for 2° latitude boxes along the

U.S. West Coast. A nonlinear trend was estimated for the monthly series using a state-space

model (Schwing and Mendelssohn in press). The 2° averaged data from the entire North

Pacific Ocean also are meaned seasonally for two decade-long periods (1966-75 and 1977-

86) to compare seasonal differences before and after a significant “climate shift” in 1976

(Trenberth 1990). This analysis places the coastal time series in a basin-scale context.

Based on the monthly time series, the U.S. West Coast can be divided into three

distinct geographical regions. The northern region (north of 40°N) features a rapid transition

from strongly equatorward to poleward wind stress with distance north (Fig. 1). The mean

stress north of 44°N is poleward and has become increasingly poleward over time. The SSTs

north of 40°N vary temporally in unison and exhibit little spatial difference in magnitude

(Fig. 2).

Winds south of 40°N are equatorward and can be described in terms of central and

southern regions (Fig. 1). The central region (32-40°N) exhibits the greatest coastal wind

stress magnitudes. This region features the greatest scales of interannual-to-decadal variation

in stress (Fig. 1) and SST (Fig. 2) as well. Stress in the southern region (22-32°N) has

become increasingly equatorward over time, like the central region, but with relatively little

interannual variation (Fig. 1). Mean SST (Fig. 2) decreases consistently with increasing
106

Figure 1. Time series of poleward wind stress trends for Comprehensive Ocean-Atmosphere

Data Set (COADS) 2° boxes. Values denote center latitude of COADS boxes.

Dashed-dotted lines represent time series from southern region (22-32°N). Solid

lines represent time series from central region (32-40°N). Bold dotted lines

represent time series from northern region (40-48°N). Bold dashed line represents

38-40°N time series.
107

Figure 2. Time series of sea surface temperature (SST) trends for Comprehensive OceanAtmosphere Data Set (COADS) 2° boxes. Values denote center latitude of

COADS boxes. Fine lines denote time series south of 40°N. bold lines denote

time series north of 40°N. Fine and bold broken lines denote time series for 38-

40°N and 42-44°N COADS boxes, respectively.
108

latitude in the central and southern regions. The SST over about 30-38°N appears to warm

rapidly in response to the 1957 and 1983 ENSO events as well as the 1976 regime shift

(Trenberth 1990).

The SSTs off Washington and Oregon, on the other hand, take several months to

years following the 1976 shift to warm by similar amounts, and they are less sensitive to

ENSO events. Although SST series exhibit a warming tendency south of 36°N, the COADS

SSTs show a cooling tendency north of 36°N (Fig. 2). However, shore-based SST trends

along the entire U.S. West Coast display a significant warming tendency over the past several

decades. A lack of correspondence between the COADS and shore SST time series north of

36° N suggests there is considerable cross-shelf as well as latitudinal variability in the

northeastern Pacific. This is confirmed by analysis of the decadal differences before and after

1976 for the North Pacific, as well as examination of COADS data in the northeastern Pacific

on 1° space scales (Schwing et al. in press).

The SST shows decadal-scale periods of warming and cooling that extend along the

entire coast. Wind stress anomalies are less coherent latitudinally and are uncorrelated with

local SST, suggesting that decadal-scale SST variability in the coastal northeastern Pacific is

controlled by the basin- to global-scale meteorological fields, rather than local wind forcing.

The decadal comparison of data over the entire basin substantiates this conclusion.

Figure 3 shows the linear trends of the poleward stress and SST time series. The

correlation between poleward stress and SST is positive in much of the central region;

increasing equatorward stress coincides with a cooling trend. Outside of the central region,

however, the trends in stress and SST are negatively correlated. Increasing equatorward stress

coincides with warming south of 34°N, while greater poleward stress accompanies a cooling

trend north of 44°N.

It is apparent that over the last several decades, surface coastal waters in the northern

portion of the California Current have either experienced a different set of forcing conditions

from those farther south, or have responded differently to large-scale atmospheric forcing.

Not only are the tendencies of wind and SST different in these regions, but the different

linear relationships between stress and SST imply that the primary mechanisms driving

variability in SST, and probably the general ocean circulation, on decadal time scales is

fundamentally different in these regions.

Preliminary analysis of decadal changes beginning in 1976 shows a strong correlation

between anomalously high wind divergence, hence greater upwelling, and cool SST in winter

over the central North Pacific. Anomalously weak divergence and warm SSTs are seen in a

broad stretch along the North American west coast. Cool anomalies propagate eastward until

they extend along the West Wind Drift to within a few degrees of the coast off Oregon and

Washington. Thus, it appears that wintertime anomalies in wind forcing over the central

Pacific, rather than changes in coastal wind, lead to the observed regional SST pattern in the

coastal northeastern Pacific. A complex interaction of spatially as well as temporally varying
109

Figure 3. Linear trends of Comprehensive Ocean-Atmosphere Data Set (COADS) poleward

stress (solid circles) and sea surface temperature (SST) (open circles) time series

along North American west coast, 22-48°N. 99% confidence intervals shown by

vertical bars (gray for stress, black for SST).
110

Ekman transport, wind mixing, and direct heating appears to be responsible for the long-term

fluctuations in SST.

The temporal and spatial variability of the physical environment of the northeastern

Pacific must be considered when analyzing changes in the biological structure of its

ecosystems. Roemmich and McGowan (1995) have found that zooplankton biomass off

southern California has decreased by 80% since the 1950s. Over a similar period, Brodeur

and Ware (1992) detected a doubling in zooplankton biomass in the Gulf of Alaska. The

results reported here show that regional differences in environmental variability have existed

in the northeastern Pacific over the last five decades; therefore, it is conceivable that

analogous differences in biological productivity, coupled with environmental variability,

have occurred as well.

The results presented here clearly demonstrate the highly variable nature of the

northeastern Pacific environment in time and space, and they argue against assuming climate

change is constant, or that it can be represented by a record from a single location. The

distinct latitudinal regionalization and cross-shelf variability of wind and SST fields has key

implications for ecosystem studies as well as fisheries management. For example, which time

series or regions are more important to study in terms of defining a salmon stock’s ocean

environment? Regional differences also mean that, over their life history, salmon face a

spatially heterogeneous, changing climate. Widespread stocks also may display a very

different long-term variability from species whose domain is limited to one of the

homogeneous regions described here. Fisheries scientists must evaluate the relative

environmental differences in each region as they pertain to the climate signal and its

variability, and compare them to a species’ distribution and behavior as a function of its life

stage in order to fully understand the consequences of climate change on populations.

The long-term trends described here cannot be described without considering changes

in seasonal patterns. Schwing and Mendelssohn (in press) demonstrated, with state-space

models, that long-term changes in the seasonal cycle of environmental time series can be

independent from interannual-to-interdecadal fluctuations. The results presented here

demonstrate the importance of evaluating the entire spectrum of temporal and spatial

variability, rather than simply at global climate scales, when examining long-term

environmental fluctuations. This will improve our understanding of the linkages between

long-term variations in atmospheric forcing and the coastal ocean’s response to this

variability on regional scales, and ultimately improve our assessment of how climate

variability impacts marine ecosystems and living marine resources.

Citations

Brodeur, R. D., and D. M. Ware. 1992. Long-term variability in zooplankton biomass in the

subarctic Pacific Ocean. Fish. Oceanogr. 1:32-38.
111

Roemmich, D., and J. McGowan. 1995. Climatic warming and the decline of zooplankton in

the California Current. Science 267:1324-1326.

Schwing, F. B., and R. Mendelssohn. In press. Increased coastal upwelling in the California

Current System. J. Geophys. Res.

Schwing, F. B., R. Mendelssohn, and R. H. Parrish. In press. Recent trends in the spatial

variability of the SST and wind fields of the California Current System. Committee

on Earth Observations Satellites (CEOS) Workshop Proceedings.

Trenberth, K. E. 1990. Recent observed interdecadal climate changes in the Northern

Hemisphere. Bull. Am. Meteorol. Soc. 71:988-993.
112
113

REGIME SCALE CLIMATE FORCING OF SALMON POPULATIONS IN

THE NORTHEAST PACIFIC—SOME NEW THOUGHTS AND FINDINGS

R. C. Francis1

 and S. R. Hare2

1

School of Fisheries

Box 357980

University of Washington

Seattle, WA 98195-7980

2

International Pacific Halibut Commission

P.O. Box 95009

University of Washington

Seattle, WA 98145-2009

Recent work (Hare and Francis 1992, Francis and Hare 1994, Hare and Francis 1995,

Hare 1996) has shown that Alaska salmon population production responds to regime-scale

(interdecadal) climate forcing, manifesting itself in low frequency and rather abrupt jumps

(Fig. 1) which correspond very closely to similar abrupt shifts in North Pacific atmosphere

and ocean climate (Fig. 2). Careful analysis reveals that

1. This connection between atmosphere/ocean physics and salmon production occurs

early in the salmon marine life history.

2. To date, connections between indices of climatic variability and salmon production

have been found at the regime (interdecadal) scale, but not at the interannual scale.

The signature of these climatic regime shifts is reflected in a number of atmospheric

and oceanic variables, the most noteworthy of which are winter sea level pressure (SLP) and

spring sea surface temperature (SST) over a large region of the North Pacific. During the

20th century, there appear to have been four interdecadal regimes (Fig. 2, top) in the coupled

atmosphere/ocean system of the North Pacific: 1900-24, 1925-46, 1947-76, 1977-present

(Francis et al. in prep., Hare 1996). The lower two panels of Figure 2 show differences in

mean winter SLP and SST between the two most recent regimes. These two patterns

characterize what we call the Pacific Decadal Oscillation which, when positive, is reflected in

a deep winter Aleutian low pressure system and a bipolar SST anomaly pattern with warm

SST anomalies along the Northeast Pacific coast and cold SST anomalies in the central

Pacific. These patterns are derived, analyzed, and discussed in detail by Hare (1996).

The objective of this paper is to discuss recent findings on the effects of regime-scale

climate changes on upper ocean dynamics and apparent responses in phytoplankton and

zooplankton production in both the California and Alaska Current regions of the Northeast
114

Figure 1. Time history (dashed lines), intervention model fits (thin solid lines), and

estimated interventions (thick solid lines) for Alaska salmon time series (from

Francis and Hare 1994).
115

Figure 2. Two indicators of large-scale, long-term climate variability over the North Pacific

in the 20th century. The top two panels show major components of variability of

North Pacific winter sea surface temperature (SST) (Pacific Decadal Oscillation,

PDO) and winter sea level pressure (SLP) along with intervention model fits. The

two bottom panels illustrate winter atmospheric and spring oceanic effects of the

1976/77 climate regime shift (Hare 1996).
116

Pacific. These results have major implications concerning mechanisms linking the observed

decadal-scale climate response of Northeast Pacific salmon to their ocean environment.

Recent Findings

A Model

Over the past few decades, a conceptual model has developed which relates

atmospheric circulation in the North Pacific to variations in biological production in the large

oceanic ecosystems (Fig. 3) of the Northeast Pacific (Ware and MacFarlane 1989). Wickett

(1967), Chelton and Davis (1982), and Chelton (1984) were the first to speculate that the

intensities of the flows in the Alaska and California Currents fluctuate in opposition to each

other. That is, when one of the currents is stronger than normal, the other is weaker. They

hypothesized that these north-south shifts in the bifurcation of the Subarctic Current (West

Wind Drift) could be forced by physical factors occurring in the western or central Pacific.

Taking this one step further, and based on marine biological indices, Hollowed and Wooster

(1992) and Francis (1993) have characterized two alternating interdecadal states of

atmospheric and oceanic circulation in the Northeast Pacific which result in very different

components of fisheries production (e.g., groundfish, salmon) in these two major coastal

domains. Hollowed and Wooster (1992) have characterized two alternating “warm” and

“cool” states lasting 6 to 12 years each. Hare and Francis (1992), Francis (1993), Francis and

Hare (1994), and Hare and Francis (1995) find similar although longer periods (25 to 35

years) of oscillating “warm” and “cool” regimes which relate very closely to the production

dynamics of Alaska salmon (Figs. 1 and 2). In addition, Francis (1993) speculated that the

interdecadal dynamics of salmon production in these two oceanic domains is inversely

correlated.

How has this model fared or changed in recent years? In what follows, we present

both biological and physical results which expand and change our understanding of how

interdecadal climate change affects the dynamics of marine biological production in the

Northeast Pacific.

Biology

Perhaps the major breakthroughs in terms of changing our thinking have related to

studies of phytoplankton and zooplankton production in the Northeast Pacific and their

responses to interdecadal climate forcing. The three major studies reported in this section

(Brodeur and Ware 1992, Polovina et al. 1995, Roemmich and McGowan 1995) focused on

changes in plankton production which occurred in response to the Northeast Pacific climatic

regime shift of 1976-77 (Miller et al. 1994).
117

Figure 3. Relevant large-scale upper-level physical oceanography of the Subarctic North

Pacific and Bering Sea (Francis and Hare 1994).
118

Venrick et al. (1987) showed significant shifts in phytoplankton production

(integrated chlorophyll a) just north of Hawaii at about the time of the 1976-77 regime shift

(Fig. 4). Subsequent analysis (Venrick 1994) revealed that his response was due to increased

phytoplankton production in deep water (75-200 m) in response to a shift in ocean mixing

and a deepening of the mixed layer. Polovina et al. (1995) further supported this and

reported, associated with the 1976-77 regime shift and intensification of the Aleutian low

pressure system, a 30-80% deepening of the winter and spring mixed layer in the Subtropical

Domain (Northwestern Hawaiian Islands) and central Transition Zone (Emperor Seamounts)

and a 20-30% shoaling of the mixed layer in the northern Subarctic Domain (Gulf of Alaska)

(Fig. 5). Based on modeling of phytoplankton response to these changes, Polovina et al.

(1995) speculated that these physical conditions would increase primary and secondary

production in the northern Subtropical and northern (central) Subarctic Domains and

decrease them in the Transition Zone.

Brodeur and Ware (1992), Brodeur et al. (1996), and Roemmich and McGowan

(1995) have shown that zooplankton production in the central Subarctic Domain (central Gulf

of Alaska) and Coastal Upwelling Domain (California Current) seems to have responded in

opposite directions to the 1976-77 regime shift. In the central Subarctic Domain, summer

zooplankton biomass more than doubled between the late 1950s and the 1980s (Brodeur and

Ware 1992, Brodeur et al. 1996, Fig. 6). The mechanism proposed to underlie the

interpretation of these phenomena involves variation in the circulation of the Subarctic Gyre

in the Northeast Pacific—a speeding up and slowing down of the Subarctic and Alaska

Currents. This would affect both Ekman pumping at the center of the gyre, leading to

increased upwelling and divergence in the center, and advection (transport of nutrients,

phytoplankton, zooplankton) around the circumference of the gyre. Associated with this

would be a shoaling of the euphotic zone (mixed layer depth) and a resultant increase in the

exposure of phytoplankton cells to light.

On the other hand, in the southern Coastal Upwelling Domain, the biomass of

macrozooplankton has decreased by as much as 70% between the early 1950s and the early

1990s (Roemmich and McGowan 1995, Fig. 7). The authors provide several mechanistic

hypotheses for their observations. First, they suggest that the coastal warming associated with

the 1976-77 regime shift may have caused increased stratification in the California Current, a

sharper thermocline with less vertical displacement of nutrient-rich waters due to wind stress

(coastal upwelling), and a resultant decrease in the fraction of the year when wind stress is

strong enough to lift nutrient-bearing waters to the sea surface near the coast. Second, they

speculate that a climate-induced shift in ocean circulation, such as the bifurcation of the west

wind drift (Subarctic Current), might import warmer water into the California Current, thus

decreasing the supply of either nutrients or the volume of zooplankton carried by the

California Current.

Both of these findings are consistent with the earlier results of Wickett (1967) who

studied the interannual variation in zooplankton volumes off California, in the western

Bering Sea, and at Ocean Station P (lat. 50°N, long. 145°W) in the central Gulf of Alaska
119

Figure 4. Index of phytoplankton in the central North Pacific (observations of integrated

chlorophyll a). Bars indicate the 95% confidence intervals of the mean; the number of observations is shown above each bar. Winter values (open squares) and

values before 1968 are excluded from the analysis (Venrick et al. 1987).
120

Figure 5. Percent change in mean winter and spring mixed layer depth (MLD) between

1977-88 and 1960-76 relative to 1960-76 levels. Shading for 1977-99 MLD which

are more than 25% deeper than 1960-76 MLD. Dashed contours are negative

values (Polovina et al. 1995).
121

Figure 6. Large-scale distribution of zooplankton biomass from sampling during the 6-week

period beginning June 1 for the period 1956-62 (top) and 1980-89 (bottom)

(Brodeur et al. 1996).
122

Figure 7. Callifornia Cooperative Oceanic Fisheries Investigations Line 90 (A) and corrected

annual averages of zooplankton volume (B) since 1950 (Roemmich and McGowan

1995).
123

during the 1950s and early 1960s. By studying the relative abundances of zooplankton in

these regions and relating them to zonal and meridional components of surface winds in a

region upstream of the bifurcation of the Subarctic Current, Wickett found that a major cause

of zooplankton variation downstream from the division point (bifurcation of the Subarctic

Current into the California and Alaska Currents) is the change in the proportion of surfacelayer, wind-driven water (Ekman transport) that is swept southward (escaping) out of the

subarctic circulation. The implication is that zooplankton and nutrients are carried with the

surface waters and that forcing conditions (surface winds) which favor a high “escapement”

of subarctic water into the California Current will increase zooplankton production in that

region and decrease it in the region of the Alaska Current.

Physics

Although there is indirect biological evidence for the ocean circulation models first

proposed by Hollowed and Wooster (1992) and Francis (1993), the physical evidence is very

hard to come by. Five recent papers do, however, begin to shed light on the issue and

speculate considerable modification to the above model. Tabata (1991), in reexamining the

Chelton and Davis (1982) premise, found a correlation between the coastal component of the

Alaska Current and California sea level, particularly during El Niño years. He attributed this

correlation, however, to the coastal currents being in phase from Canada to California rather

than to changes in the bifurcation of the Subarctic Current. Kelly et al. (1993) analyzed seasurface height anomalies for the Northeast Pacific over a 2.5-year period. Their results tended

to support those of Chelton and Davis (1982) that the California and Alaska Current systems

fluctuate “out of phase,” coinciding with variations in wind-stress curl in the North Pacific

and subsequent diversion of flow from the Alaska Gyre into the California Current as well as

with some aspects of El Niño Southern Oscillation (ENSO) dynamics. Van Scoy and Druffel

(1993), in an analysis of tritium (3

H) concentrations in seawater from Ocean Station P and a

station in the southern California Current, suggested increased advection of subpolar water

into the California Current during non-El Niño years and that ventilation of the Alaska Gyre

(intensification) occurs during El Niño years. Lagerloef (1995), in his analysis of dynamic

topography in the Alaska Gyre during 1968-90, suggested that after the well-documented

climatic regime shift of the late 1970s, the Alaska Gyre was centered more to the east and its

circulation appeared weaker after the shift than before. The implication is that the

intensification of the winter Aleutian low pressure system associated with the regime shift

did not result in a spinup of the Alaska Gyre. Finally, Miller (1996) reviews some recent

advances in large-scale modeling of the California Current and its interaction with basinscale circulation and forcing. He reports the significant deepening of the thermocline off

California after the 1976-77 regime shift (similar to Roemmich and McGowan 1995) and

attributes this to basin-scale changes in wind-stress curl. This is achieved at two time

scales—the first at the decadal and North Pacific Gyre scale forced by significant deepening

and weakening of the Aleutian low pressure system, and the second at the interannual ENSO

scale forced by waves propagating through the ocean from the tropics.
124

Figure 8. Top: Observed temperature anomalies averaged over the region long. 130-120°W,

lat. 25-45°N from the surface to 300-m depth from 1970-88. Contour interval is

0.1°C with darker shades cooler and lighter shades warmer. Bottom: Depth

anomalies (solid) of model isopycnal layer (s 24.7) at a grid point off the California

coast. Positive anomalies indicate a deeper thermocline at mean depth of roughly

180 m. Local wind-stress curl anomalies (dotted) at the same point (Miller et al.

1996).
125

Miller et al. (1996) and Miller (1996) support the findings of Roemmich and

McGowan (1995) and report both decadal and interannual signals in the dynamics of the

thermocline off the California coast (Fig. 8). The first signal is a thermocline deepening

associated with decadal-scale changes in the subtropical gyre and its mixed layer structure as

influenced by changes in gyre-scale wind forcing (wind-stress curl). The second signal

occurs at the ENSO time scale (3-7 years) and is driven by waves propagating through the

ocean, presumably from the tropics. One can see the effects of both of these processes in the

dynamics of mixed layer temperature profiles as well as thermocline depth anomalies (Fig.

8). The results of Enfield and Allen (1980) tend to support this and indicate that the region

off central California (San Francisco) may be a dividing point between locations to the south

where sea level is influenced by anomalies of equatorial origin (related to fluctuations in the

Southern Oscillation) and locations to the north where sea level is influenced strongly by

local wind-stress anomalies resulting from energetic winter storms (related to the winter

Aleutian low pressure phenomenon). Therefore, the higher frequency dynamics in mixed

layer depth and temperature reported by Miller et al. (1996) and Miller (1996) for a region off

southern California (Fig. 8) may not be as evident in more northerly components of the

California Current. In fact, Freeland (1990) reported that coastal British Columbia sea surface

temperatures showed very little coherence with the ENSO signal.

Finally, Miller (1996) also reported that after the 1976-77 regime shift there appeared

to be a stronger than normal northward flow into the central Gulf of Alaska but little change

in (flow into) the California Current system.

Discussion

Clearly much has been learned since 1982 (when Chelton first proposed his model)

concerning the relation between atmosphere/ocean physics and Northeast Pacific salmon

production. Based on the results summarized above, the following seems fairly clear:

1. The major climate influence on salmon production occurs at the decadal time scale,

early in the marine life history, and in a bottom-up fashion through physical

influences on primary and secondary production.

2. Plankton production seems to be influenced at the decadal (regime) scale by major

climate-induced changes in the structure of the mixed layer. These influences appear

to operate in opposite directions in the California Current and Alaska Current oceanic

domains.

3. The farther south, the stronger is the influence of climate on biological production at

the higher-frequency ENSO scale. For example, the coastwide spike in Pacific

Northwest salmon production which seemed to affect cohorts entering the ocean

either in late 1984 or early 1985 could have resulted from a 1985 rebound to the
126

1982-83 El Niño (Fig. 8—rapid cooling of the ocean and corresponding deepening of

the mixed layer off California in 1985).

4. The effects of ocean circulation, particularly as they relate to the relative intensities of

advection of subarctic water into the California and Alaska Currents, are less clear.

Recent evidence points to a more complicated picture than the first speculated by

Chelton (1984) at the first of these conferences in 1983. What does appear to be

happening is that if advection and circulation are important, it is their effects on upper

ocean structure (mixed layer depth, temperature) which, in turn, directly affects

biological production.

Citations

Brodeur, R. D., B. W. Frost, S. R. Hare, R. C. Francis, and W. J. Ingraham. 1996. Interannual

variations in zooplankton biomass in the Gulf of Alaska and covariation with

California Current zooplankton. CalCOFI (Calif. Coop. Oceanic Fish. Invest.) Rep.

37:80-99.

Brodeur, R. D., and D. M. Ware. 1992. Long-term variability in zooplankton biomass in the

Subarctic Pacific Ocean. Fish. Oceanogr. 1:32-38.

Chelton, D. B. 1984. Commentary: Short-term climatic variability in the Northeast Pacific

Ocean. In W. G. Pearcy (editor), The influence of ocean conditions on the production

of salmonids in the North Pacific, p. 87-99. Oregon Sea Grant Program, Oregon State

Univ., Corvallis. Publ. ORESU-W-83-001.

Chelton, D. B., and R. E. Davis. 1982. Monthly mean sea level variability along the western

coast of North America. J. Phys. Oceanogr. 12:757-784.

Enfield, D. B., and J. S. Allen. 1980. On the structure and dynamics of monthly mean sea

level anomalies along the Pacific Coast of North and South America. J. Phys.

Oceanogr. 10:557-578.

Francis, R. C. 1993. Climate change and salmonid production in the North Pacific Ocean. In

K. T. Redmond and V. L. Tharp (editors), Proceedings of the Ninth Annual Pacific

Climate (PACLIM) Workshop, p. 33-43. Calif. Dep. Water Resour. (Available from

California Department of Water Resources, 1416 Ninth St., Rm. 1104-1, Sacramento,

CA 95814.)

Francis, R. C., and S. R. Hare. 1994. Decadal-scale regime shifts in the large marine

ecosystems of the North-east Pacific: A case for historical science. Fish. Oceanogr.

3:279-291.
127

Francis, R. C., S. R. Hare, A. B. Hollowed, and W. S. Wooster. In prep., Effects of

interdecadal variability on the oceanic ecosystems of the Northeast Pacific.

(Submitted to J. Climate.)

Freeland, H. J. 1990. Sea surface temperatures along the coast of British Columbia: Regional

evidence for a warming trend. Can. J. Fish. Aquat. Sci. 47:346-350.

Hare, S. R. 1996. Low frequency climate variability and salmon production. Ph.D. Thesis,

School of Fisheries, University of Washington, Seattle, 306 p.

Hare, S. R., and R. C. Francis. 1992. An intervention analysis approach to modelling the

linkage between Northeast Pacific regime shifts and Alaska salmon production,

p. 135-163. In Salmon management in the 21st century, Proceedings of the 1992

Northeast Pacific Chinook and Coho Workshop. Idaho Chapter of American Fisheries

Society, Boise, Idaho.

Hare, S. R., and R. C. Francis. 1995. Climate change and salmon production in the Northeast

Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations, p. 357-372. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Hollowed, A. B., and W. S. Wooster. 1992. Variability of winter ocean conditions and strong

year classes of Northeast Pacific groundfish. Int. Counc. Explor. Sea Mar. Sci. Symp.

195:433-444.

Kelly, K. A., M. J. Caruso, and J. A. Austin. 1993. Wind-forced variations in sea surface

height in the Northeast Pacific Ocean. J. Phys. Oceanogr. 23:2392-2411.

Lagerloef, G. S. E. 1995. Interdecadal variations in the Alaska Gyre. J. Phys. Oceanogr.

25:2242-2258.

Miller, A. J. 1996. Recent advances in California Current modeling. CalCOFI (Calif. Coop.

Oceanic Fish. Invest.) Rep. 37:69-79.

Miller, A. J., D. R. Cayan, T. P. Barnett, N. E. Graham, and J. M. Oberhuber. 1994. The

1976-77 climate shift of the Pacific Ocean. Oceanography 7:21-26.

Miller, A. J., D. R. Cayan, and W. B. White. 1996. Mechanisms of upper-ocean thermal

variability in a 1970-1988 simulation and observations. In C. M. Isaacs and V. L.

Tharp (editors), Proceedings of the Twelfth Annual Pacific Climate (PACLIM)

Workshop, p. 19-32. Calif. Dep. Water Resour. Tech. Rep. 46.

Polovina, J. J., G. T. Mitchum, and G. T. Evans. 1995. Decadal and basin-scale variation in

mixed layer depth and the impact on biological production in the Central and North

Pacific, 1960-88. Deep-Sea Res. 42(10):1701-1716.
128

Roemmich, D., and J. McGowan. 1995. Climate warming and the decline of zooplankton in

the California Current. Science 267:1324-1326.

Tabata, S. 1991. Annual and interannual variability of baroclinic transports across Line P in

the northeast Pacific Ocean. Deep-Sea Res. 38(Suppl. 1):S221-S245.

Van Scoy, K. A., and E. R. M. Druffel. 1993. Ventilation and transport of thermocline and

intermediate waters in the northeast Pacific during recent El Niños. J. Geophys. Res.

98(C10):18083-18088.

Venrick, E. L. 1994. Scales of variability in a stable environment: Phytoplankton in the

Central North Pacific. In T. M. Powell and J. H. Steele (editors), Ecological time

series, Chapter 10. Chapman and Hall, New York.

Venrick, E. L., J. A. McGowan, D. R. Cayan, and T. L. Hayward. 1987. Climate and

chlorophyll a: Long-term trends in the central North Pacific Ocean. Science 238:70-

72.

Ware, D. M., and G. A. McFarlane. 1989. Fisheries production domains in the Northeast

Pacific Ocean, p. 359-379. In R. J. Beamish and G. A. McFarlane (editors), Effects of

ocean variability on recruitment and an evaluation of parameters used in stock

assessment models. Can. Spec. Publ. Fish. Aquat. Sci. 108.

Wickett, W. P. 1967. Ekman transport and zooplankton concentration in the North Pacific

Ocean. J. Fish. Res. Board Can. 24(3):581-594.
129
130
131

Process and Mechanisms—Estuarine
132
133

THE RELATIONSHIP OF ESTUARINE PRIMARY AND SECONDARY

PRODUCTIVITY TO SALMONID PRODUCTION: BOTTLENECK OR

WINDOW OF OPPORTUNITY?

Charles A. Simenstad

Coordinator, Wetland Ecosystem Team

School of Fisheries

University of Washington

Box 357980

Seattle, WA 98195-7980

The Issue

Concepts such as “window of opportunity” and “bottleneck” have been given survival

significance in estuaries since we first began evaluating that phase of Pacific salmon

(Oncorhynchus spp.) early life histories. Estuarine windows of opportunity and bottlenecks

both refer to the influence of estuarine conditions (e.g., food, predators, physicochemical

conditions affecting physiology and performance, etc.) to enhance or detract from overall

survival disproportional to influences in fresh water or the ocean. Early salmon management,

and particularly salmon hatchery release policies which generally sought to hold fish to a size

and time that minimized estuarine utilization, tended to consider estuaries as “sinks,”

contributing more to juvenile salmon mortality than survival; despite contrary evidence, these

attitudes and practices still persist in many governmental and private salmon hatcheries.

These concepts are more recently represented in management paradigms promoting artificial

enhancement and manipulation (e.g., salmon hatchery releases) that can be controlled

“adaptively” in comparative real time to take advantage of estuarine conditions in order to

maximize survival and buffer poor ocean conditions. In employing any of these concepts, we

imply that favorable conditions for juvenile salmon rearing in estuaries are “scheduled” or

reach some “optimum” or “convergence” that may dictate survival to return as adults. This

issue avoids the question of whether the effect of estuarine productivity is independent of

other mortality factors in the sequential salmon life history continuum, or whether there are

either compensatory or depensatory relationships between estuarine factors and those

affecting freshwater and ocean survival.

One factor commonly considered to regulate salmon survival in estuaries is the

availability of prey resources; that is, that food carrying capacity is often limiting and that

juvenile salmon have evolved to take advantage of maximal periods of estuarine productivity.

This might be considered the “bottom-up” regulation of overall salmon production by some

average quantity and timing of primary producers and consumers supporting estuarine food

webs utilized by juvenile salmon. This is somewhat contrary to the observation that Pacific

salmon populations, with their relatively long numerical response times, have evolved

diverse life history strategies (types, races, tactical). These strategies compensate for
134

environmental variation across time and space scales through their entire life cycle, and will

tend to average out high frequency components of environmental variation (e.g., interannual/

freshwater-estuarine-marine), and respond to low frequency components of variability

affecting salmon survival (e.g., oceanic regime shifts). It is also important to realize that

“top-down” influences, in which predation or competition independent of salmon size or

density prevail, may be just as valid a regulator of salmon production.

A bottom-up view of salmon production in estuaries also assumes that the quantity or

quality of food can directly or indirectly limit survival—directly by reducing growth and

increasing size-dependent mortality, and indirectly by altering salmon behavioral responses

(e.g., migration patterns and rates) that increase their risk to mortality agents such as

predators. Understanding spatial and temporal variability in the availability of food

organisms, as well as the food web processes that support them, might provide a view into

comparable variability in salmon survival. Unfortunately, our appreciation of the effects of

estuarine variability have not advanced measurably since reviewed in the predecessor

workshop in 1983 (Levings 1984, Levy 1984, Simenstad and Wissmar 1984). While we have

a marginally better understanding of the structure and processes in estuarine food webs that

contribute to salmon production, there has really been no advancement in our understanding

of the spatial and temporal variability in food web linkages to salmon or of the response by

individual salmon or their populations to this variability.

Estuaries as Pulsed Ecosystems

The essence of estuaries is that they are extremely variable, pulsed ecosystems; the

quantity, composition, timing, and rate of primary and secondary production processes

supporting juvenile salmon varies extensively over space and time. Juvenile salmon

themselves pulse through the systems, although now perhaps at more punctuated frequencies

than in prehatchery eras. Because of the relative independence of many factors regulating the

dynamics of juvenile salmon migrations through estuaries and the production of prey

organisms and associated food web processes, overlap and coincidence of salmon with peak

prey resource availability are likely to be random and uncoupled.

Food webs of estuaries in the Pacific Northwest are based predominantly on detritus,

but the composition of organic matter contributing to the estuarine detritus pool may vary

significantly depending upon location (e.g., ecoregion), extent and type of watershed and

estuary, climate, geology, and oceanic energy regime, among many factors. Comprehensive,

estuary-scale accounting of organic matter production and consumption has not been

attempted for many estuaries in the region, but annual carbon input budgets have been

calculated for three contrasting estuaries: Hood Canal (Simenstad and Wissmar 1985), Grays

Harbor (Thom 1981, 1984), and the Columbia River estuary (Simenstad et al. 1990). Not

surprisingly, given the considerably greater extent of the Columbia River watershed, the total

annual loading of organic carbon to that estuary is about five orders of magnitude greater

than either Hood Canal or Grays Harbor (Fig. 1a). While import of fluvial organic matter

dominates both the Columbia River estuary (87.2%) and Grays Harbor (80.1%) carbon

budgets, phytoplankton (59.7%), and benthic algae (29.7%) contribute much more to the

Hood Canal budget, and eelgrass production is of significance (11.3%) primarily in Grays
135

Figure 1. Variability in annual production (kg C yr-1) (A) and of contribution of organic

matter sources (B) to three estuaries in the Pacific Northwest: Hood Canal, a fjord

adjoining Puget Sound, with numerous deltaic subestuaries; Grays Harbor, a large

euhaline, flooded-river-valley coastal estuary; and the Columbia River estuary, a

freshwater-dominated estuary with the largest and most diverse watershed in the

region.
136

Harbor; emergent marsh production is comparatively insignificant (1.4-4.8%) in all three

systems (Fig. 1b).

However, delivery of these different organic matter constituents to the estuarine food

web is neither proportional nor coincident to the source inputs. The quality of organic matter

is fundamentally more important than bulk organic contribution to the estuary, implying that

the sources of organic matter to the estuarine detritus pool may be more important than the

bulk delivery. Terrestrial and marsh detritus tends to be much more refractory, and less

efficiently incorporated into the estuarine food web, than phytoplankton and benthic algae.

Riverine input tends to correspond to river discharge, peaking with winter storms and spring

snowmelt, while organic matter from eelgrass production enters the estuary in late winter,

benthic algae and phytoplankton in mid-summer, and emergent marsh in the fall (Fig. 2;

Thom 1987). Some food web pathways may be almost immediate, as suggested for the

incorporation of estuarine foam into littoral flat consumers (Wissmar and Simenstad 1984).

Deterministic Food Web Linkages

Irrespective of the variation in quantity, quality, and timing of organic matter

contributing to the food web, we continue to accumulate evidence that certain species and life

history stages of juvenile salmon focus their foraging in estuaries on certain types of prey,

which in some cases may be an important factor determining estuarine residence time and

growth (Wissmar and Simenstad 1988). Results from our on-going studies of juvenile salmon

use of estuarine wetlands in Puget Sound and coastal Washington continue to sustain earlier

interpretations that certain salmon species and life history types (e.g., chum salmon, O. keta,

and subyearling chinook salmon, O. tshawytscha) prey selectively on specific benthic or

epibenthic organisms, such as amphipods (Corophium spp.) and harpacticoid copepods

(Harpacticus uniremis, Tisbe sp.) (Simenstad et al. 1988; Wissmar and Simenstad 1988). If

we have acquired any additional understanding, it is from tidal freshwater and brackish

wetlands, where we also find juvenile salmon (subyearling chinook and coho, O. kisutch)

feeding concentrated on emergent marsh and riparian insects (e.g., chironomids, aphids)

(Shreffler et al. 1992; Miller 1993; Simenstad et al. 1992, 1993, in press; Miller and

Simenstad in revision).

Variations in Estuarine Food Webs

Supporting Juvenile Salmon

One recent tool that is providing a more powerful identifier of estuarine food web

variability is the use of stable natural isotopes, and particularly multiple isotopes (e.g., δ 13C,

δ 15N, δ 34S) because significant overlap can occur among isotopic signatures of different
137

Figure 2. Fluctuations in the input of organic matter to Grays Harbor for different watershed

and estuarine sources (From Thom 1981, 1987).
138

organic sources for any one isotope (e.g., differentiating terrestrial inputs from brackish

marsh would be impossible without coupling δ 34S with δ 13C; addition of δ 13C further

distinguishes trophic level shifts). While δ 13C analyses of food web sources and pathways

have been used to investigate a variety of estuarine systems (e.g., Hood Canal, Simenstad and

Wissmar 1985; Padilla Bay, Puget Sound, Simenstad and Wissmar 1985; Fraser River

estuary, Levings 1994; Willapa Bay and Columbia River estuary, C. Simenstad, unpubl. data,

School of Fisheries, University of Washington, Box 357980, Seattle, WA 98195-7980), the

addition of δ 15N has been incorporated for a few of those systems (Padilla Bay, Fraser River)

and δ 34S has been added for only Willapa Bay and the Columbia River estuary.

As more data from stable isotope studies in these different estuaries emerge, it is

becoming apparent that organic matter production and food web processes supporting

juvenile salmon production differ across estuaries, often irrespective of seemingly

deterministic food web pathways. For instance, δ 13C of epibenthic harpacticoid copepods

and amphipods may vary by as much as 11‰ (-9‰ to -20‰), and the same species,

Corophium salmonis, can differ by as much as 5.5‰ in adjacent estuaries (Willapa Bay, -

18.9‰ vs. Columbia River estuary, -24.4‰). Spatial variation within the same estuary is also

evident, as indicated by a wide range in δ 13C of chinook salmon fry (approximately 20‰ to -

30‰) and narrow range (approximately -34‰ to -36‰) for coho salmon presmolts found in

the lower Fraser River (Levings 1994), and -19.8‰ for the calanoid copepod Eurytemora

affinis in the brackish channels of the Columbia River estuary vs. -29.9‰ from the estuarine

turbidity maxima in the portion of the same estuary with varying salinities (Simenstad,

unpubl. data, School of Fisheries, University of Washington, Box 357980, Seattle, WA

98195-7980); where the δ 15N signature, 7.4, did not differ at all between these samples).

These preliminary indicators of food web pathway variability suggest that both differential

pulses of organic matter and heterogeneous distributions of the material across an estuary

may account for dramatically different trophic support of secondary consumers such as

salmon, especially when salmon localize their rearing and migrations in a specific estuarine

region or habitat.

Responses by Salmon to Variability

in Estuarine Production

As described in the predecessor workshop in 1983 (Levings 1984; Levy 1984;

Simenstad and Wissmar 1984), the issue of carrying capacity limitations for juvenile salmon

still remains an untested enigma. Few studies have attempted to describe juvenile salmon

production, much less survival, relative to temporal and spatial variability in estuarine

biochemical conditions, and most of these are prior to 1983. The descriptive comparisons of

juvenile fall chinook salmon relative abundance and size in 11 Oregon estuaries in 1977-82

by Herring and Nicholas (1983) still remains one of the few comparisons between salmon

use and estuarine structure. Across the distribution of estuary (at mean lower low water) area,

from 6,180 ha for Coos Bay to 90 ha for the Chetco River estuary (Fig. 3a), they found a

trend in increasing catch per unit effort (CPUE) and decreasing mean fish size (Fig. 3b),

although considerable variability in these trends was also evident. Interannual variation was
139

Figure 3. Surface areas of 11 Oregon estuaries (A) (Oregon Division of State Lands 1973)

relative to the catch per unit effort (CPUE) and mean fork length of juvenile

chinook salmon (B) (Nicholas and Hankin 1988).
140

also prevalent within the inverse estuary area/fish length relationship (Fig. 4). Suggestion of a

density-dependent limitation on fish growth and production (assuming equal emigration and

immigration rates), as indicated by fish length, was implicated beyond a CPUE threshold of

about 10 to 20 fish per set (Fig. 5). This may coincide with observations from 16 British

Columbia estuaries between 1970 and 1982 (Levings 1984) and our own comprehensive

estuarine catch data (C. Simenstad, unpubl. data, School of Fisheries, University of

Washington, Box 357980, Seattle, WA 98195-7980) that it is rare to find juvenile chinook

salmon densities higher than about 1.0 fish m-2. The implications of an estuarine carrying

capacity, as modulated by salmon life history type and timing of estuarine entry, is still

sustained principally by Reimer’s (1973) seemingly ageless study of the survival of chinook

salmon life history type in the Sixes River estuary, which we still have yet to repeat or

expand upon for any other estuaries.

Conclusions

While the paradigm of detritus-based estuarine food webs may still be generally

applicable across salmonid ecosystems, the actual food web processes supporting specific

salmonid prey may not be as indicative of broad-based detritus inputs. Factors regulating the

production of primary consumers may not necessarily depend on the availability of food

resources; while there appear to be chronosequences of benthic/epibenthic prey community

structure and production, considerable temporal and spatial variability prevail. Production of

key prey species distributed across estuarine gradients, such as insects (chironomids; tidal

freshwater-brackish), amphipods (Corophium spp., brackish-mesohaline), and harpacticoid

copepods (Harpacticus uniremis, Tisbe sp.; salinities varying from 5 ppt to over 30 ppt) may

not be coincident, and not necessarily linked to processes (natural, or anthropogenically

“managed”) that regulate juvenile salmon entry, residence, and survival in the estuary.

Alternatively, both physical (inflow, temperature) and biological (primary production,

predation) factors that affect juvenile salmon and their prey production may be Aoptimal@

during estuarine residence, but may not coincide with subsequent ocean conditions. Diversity

in Pacific salmon species, racial, and tactical life history strategies, which has likely declined

under historic exploitation and management, may offer one clue of the salmon’s evolutionary

solution to such variability in estuarine conditions.

Ultimately, we must recognize that increased knowledge about the influence of

dynamic ecosystems such as estuaries on salmon is more likely to elucidate the constraints

upon alternative salmon management strategies rather than predictable relationships that can

be used to Atake advantage@ of estuaries. As pointed out by Levings (1984), it may be entirely

unrealistic to use production at lower trophic levels as indicators of estuarine (juvenile

Mesohaline is defined as waters of 5-18 ppt.
141
142
143

salmon) production potential given the variability in fish Adependence@ on specific prey or

the spatial distribution of prey.

From salmon biologists’ perspectives, ecosystem management of salmon must

ultimately deal with managing man’s adverse impacts on critical ecosystem processes, and

within the scope of natural variability, rather than managing ecosystems per se.

Understanding the scope of salmon population responses to estuarine variability will require

considerably more focused and intense research into issues such as the following: 1) links

between variation in estuarine organic matter production and consumer population dynamics,

2) whether pulses of salmon prey resources are interlinked with salmon behavior,

3) relationships between organic matter quality (sources) and consumer (salmon prey)

production, 4) variation in juvenile salmon estuarine entry, residence time, growth and

mortality, and relationship to primary and secondary food web pulses, 5) effect of life history

diversity on estuarine-ocean variability, and 6) the presence or lack of interdependence

between estuarine survival and ocean survival.

Citations

Levings, C. D. 1984. Commentary: Progress in attempts to test the null hypothesis that

juvenile salmonids aren’t dependent on estuaries. In W. G. Pearcy (editor), The

influence of ocean conditions on the production of salmonids in the North Pacific: A

workshop, p. 287-296. Oregon State Univ., Corvallis, OR. Sea Grant Col. Prog.,

ORESU-W-83-001.

Levings, C. D. 1994. Life on the edge: Structural and functional aspects of chinook and coho

salmon rearing habitats on the margins of the lower Fraser River. In Salmon

ecosystem restoration: Myth and reality, Proceedings of 1994 Northeast Pacific

Chinook and Coho Salmon Workshop, p. 139-147. Oregon Chapter, Am. Fish. Soc.,

Corvallis, OR.

Levy, D. A. 1984. Commentary: Variations in estuary utilization among juvenile chinook

salmon populations. In W. G. Pearcy (editor), The influence of ocean conditions on

the production of salmonids in the North Pacific: A workshop, p. 297-302. Oregon

State Univ., Corvallis, OR. Sea Grant Col. Prog., ORESU-W-83-001.

Miller, J. A. 1993. Juvenile chinook (Oncorhynchus tshawytscha) and coho (O. kisutch)

salmon in natural and created estuarine habitats: Foraging and daily growth. M.S.

Thesis, Univ. Washington, Seattle, WA, 84 p.

Miller, J. A., and C. A. Simenstad. In prep. Juvenile chinook and coho salmon use of a

natural and created estuarine slough on the Chehalis River, WA: Short-term growth,

residence, and foraging. Estuaries.
144

Nicholas, J. W., and D. G. Hankin. 1988. Chinook salmon populations in Oregon coastal

river basins: Description of life history and assessment of recent trends in run

strengths. Oregon Dept. Fish Wildl., Info. Rep. 88-1, 359 p.

Oregon Division of State Lands. 1973. Oregon estuaries. Salem, OR, 48 p.

Reimers, P. E. 1973. The length of residence of juvenile fall chinook in the Sixes River,

Oregon. Fish. Comm. Oreg. Res. Rep. 4(2):3-42.

Sherwood, C. R., D. A. Jay, R. B. Harvey, P. Hamilton, and C. A. Simenstad. 1990.

Historical changes in the Columbia River estuary. Prog. Oceanogr. 25:299-357.

Shreffler, D. K., C. A. Simenstad, and R. M. Thom. 1992. Foraging by juvenile salmon in a

restored estuarine wetland. Estuaries 15:204-213.

Simenstad, C. A., J. R. Cordell, W. G. Hood, B. E. Feist, and R. M. Thom. In press.

Ecological status of a created estuarine slough in the Chehalis River estuary:

Assessment of created and natural estuarine sloughs, January-December 1995. Fish.

Res. Inst., School Fish., Univ. Wash., Seattle, WA, 81 p.

Simenstad, C. A., J. R. Cordell, W. G. Hood, J. A. Miller, and R. M. Thom. 1992. Ecological

status of a created estuarine slough in the Chehalis River estuary: Report of

monitoring in created and natural estuarine sloughs, January-December 1991. FRIUW-9206. Fish. Res. Inst., Univ. Wash., Seattle, WA, 49 p.

Simenstad, C. A., J. R. Cordell, J. A. Miller, W. G. Hood, and R. M. Thom. 1993. Ecological

status of a created estuarine slough in the Chehalis River estuary: Assessment of

created and natural estuarine sloughs, January-December 1992. FRI-UW-9305. Fish.

Res. Inst., Univ. Wash., Seattle, WA, 56 p.

Simenstad, C. A., J. R. Cordell, R. C. Wissmar, K. L. Fresh, S. Schroder, M. Carr, and M.

Berg. 1988. Assemblages structure, microhabitat distribution, and food web linkages

of epibenthic crustaceans in Padilla Bay National Estuarine Research Reserve,

Washington. NOAA Tech. Rep. Ser. OCRM/MEMD, FRI-UW-8813, Fish. Res. Inst.,

Univ. Wash., Seattle, WA, 60 p.

Simenstad, C. A., C. D. McIntire, and L. F. Small. 1990. Consumption processes and food

web structure in the Columbia River estuary. Prog. Oceanogr. 25:271-298.

Simenstad, C. A., and R. C. Wissmar. 1984. Variability of estuarine food webs and

production may limit our ability to enhance Pacific salmon (Oncorhynchus spp.). In

W. G. Pearcy (editor), The influence of ocean conditions on the production of

salmonids in the North Pacific: A workshop, p. 272-286. Oregon State Univ.,

Corvallis, OR. Sea Grant Col. Prog., ORESU-W-83-001.
145

Simenstad, C. A., and R. C. Wissmar. 1985. δ 13C evidence of the origins and fates of

organic carbon in estuarine and nearshore marine food webs. Mar. Ecol. Prog. Ser.

22:141-152.

Thom, R. M. 1981. Primary productivity and carbon input to Grays Harbor estuary,

Washington. Grays Harbor and Chehalis River Improvements to Navigation

Environmental Studies. Final Report to U.S. Army Corps of Engineers, Seattle

District, Seattle, WA, 71 p. (Available from U.S. Army Corps of Engineers, Seattle

District Office, 4735 E. Marginal Way S., Seattle, WA 98134.)

Thom, R. M. 1984. Primary production in Grays Harbor estuary, Washington. Bull. Southern

California Acad. Sci. 83:99-105.

Thom, R. M. 1987. The biological importance of Pacific Northwest estuaries. Northwest

Environ. J. 3:21-42.

Wissmar, R. C., and C. A. Simenstad. 1984. Surface foam chemistry and productivity in the

Duckabush River estuary. In V. Kennedy (editor), The estuary as a filter, p. 331-348. 

Academic Press, Orlando, FL.

Wissmar, R. C., and C. A. Simenstad. 1988. Energetic constraints of juvenile chum salmon

(Oncorhynchus keta) migrating in estuaries. Can. J. Fish. Aquat. Sci. 45:1555-1560.
146
147

ESTUARINE SURVIVAL OF SALMONIDS: THE IMPORTANCE OF

INTERSPECIFIC AND INTRASPECIFIC PREDATION AND COMPETITION

Robert L. Emmett

National Marine Fisheries Service

Northwest Fisheries Science Center

2030 SE Marine Science Drive

Newport, OR 97365

and

Oregon State University

Department of Fish and Wildlife

Corvallis, OR 97331

Declining salmonid runs on the west coast of North America are a result of many

factors, including habitat destruction, hydropower development, overharvest, and illconceived hatchery practices. One factor that has received little attention is inter- and

intraspecific predation and competition in estuaries. Populations of salmonid predators and

possible competitors in estuaries have increased dramatically since the 1970s. In particular,

estuarine populations of marine mammals and piscivorous birds have increased significantly.

The purpose of this paper is to review the status of salmonid predators and competitors in

West Coast estuaries, highlighting current data gaps about these problems.

Predators

Since enactment of the Marine Mammal Protection Act of 1972, Northwest

populations of California sea lions (Zalophus californianus) and harbor seals (Phoca

vitulina) have increased steadily and are now healthy, productive, and growing. Many

salmonid populations, on the other hand, are unproductive and decreasing, and some are

listed as threatened or endangered under the federal Endangered Species Act (Snake River

spring/summer and fall chinook salmon (Oncorhynchus tshawytscha), Snake River sockeye

salmon (O. nerka), and Sacramento River winter chinook salmon).

Estuaries are excellent habitat for marine mammals, providing protected haul-out sites

and a high abundance of a variety of prey species, including salmonids. However, the degree

to which marine mammals prey upon salmonids is poorly understood. Harmon et al. (1994)

documented a relatively high prevalence of marine mammal tooth and claw abrasions on

adult salmonids passing Lower Granite Dam on the Snake River from 1990 to 1993. These

were mostly attributed to sea lions. Their data plus more recent data (Table 1) indicate that,

although the prevalence of marine mammal attacks are relatively high, there are no obvious
148

Table 1. Prevalence of marine mammal tooth and claw abrasions on chinook salmon

(Oncorhynchus tshawytscha) and steelhead (O. mykiss) at Lower Granite Dam on

the Snake River.*

* Data from Jerry Harmon, National Marine Fisheries Service, Northwest Fisheries Science

Center, 2725 Montlake Blvd. E, Seattle, WA 98112-2097.
149

trends. As marine mammal populations have continued to grow, prevalence of tooth and claw

abrasions has not. Moreover, these data provide no information on how many salmonids were

actually caught and consumed, nor how many died migrating to Lower Granite Dam (720 km

from the mouth of the Columbia River). What these data indicate is that marine mammals do

attack and eat salmonids and that there are factors in addition to salmon and marine mammal

population abundance that influence marine mammal attacks.

California sea lions

The West Coast California sea lion population is growing rapidly with no indications

that it is reaching an optimal sustainable population (OSP) level (i.e., an asymptotic

population exponential growth curve). From 1975 to 1994, pup counts of sea lions in

California increased at an annual rate of 5.2% and increased regionally 8% per year (Barlow

et al. 1995, U.S. Dep. Commer. in prep.). In 1992, sea lion populations were estimated to be

approximately 11,000, 17,000, and 30,000 along the coasts of Oregon, Washington, and

California, respectively. Total U.S. population of California sea lions was estimated to be

between 161,000 and 181,000 in 1994.

Although sea lion food habit studies have provided information on the occurrence of

salmonid parts in sea lion diets, most studies have not estimated how many salmonids were

consumed. The best evidence for severe marine mammal predation on adult salmonids comes

from the Ballard Locks in Seattle, Washington, where the California sea lions have been

estimated to consume about 40% of the steelhead (O. mykiss) run since 1985/1986 (U.S. Dep.

Commer. in prep.).

In the Columbia River, sea lions feed primary on fishes other than salmonids, such as

eulachon (Thaleichthys pacificus), lamprey (Lampetra spp.), Pacific herring (Clupea pallasi),

rockfish (Sebastes spp.), and northern anchovy (Engraulis mordax). Nevertheless, salmonids

may contribute substantially to the sea lion diet at specific times and locations. There also

appear to be more salmonids in the diet now (28% in the 1990s vs. 13% in the 1980s), but

this may be a result of improved laboratory procedures (U.S. Dep. Commer. in prep.).

Other feeding studies have been conducted off Cascade Head, Oregon; Rogue River,

Oregon; and the Russian River, California. At Cascade Head, mackerel, Pacific herring,

skates (Raja spp.), cephalopods, spiny dogfish (Squalus acanthias), Pacific sand lance

(Ammodytes hexapterus), rockfish, and northern anchovy were the primary prey, with 33% of

the samples containing salmonid remains. In the Rogue River (Roffe and Mate 1984),

lamprey were the dominant prey, with steelhead comprising 19% and chinook salmon 3% of

the diet by weight. Hanson (1993) found California sea lions were efficient salmonid

predators, with a catch rate (number of successful captures/number of attack attempts) of

74% at the mouth of the Russian River. Roffe and Mate (1984) calculated that sea lions

consumed less than 1% of the spring chinook run and less than 5% of the summer steelhead

run in the Rogue River. More research is needed to identify the relationship between
150

salmonid run sizes, alternative prey populations, and the number of salmonids eaten by sea

lions. Sea lion populations have increased dramatically since 1977/1978, when Roffe and

Mate performed their research. It would be valuable to repeat their study.

Harbor seals

In 1977, an estimated 100 harbor seals resided in the Columbia River estuary during

May/June, although there are now over 900 (Fig. 1). These are probably minimum estimates

because many adults migrate to adjacent estuaries during May/June to pup. Highest numbers

in the Columbia River are usually in the fall, winter, and early spring, especially during the

annual eulachon run.

Northwest harbor seal populations are growing about 7% per year, with no indications

when they will reach OSP level. Only an estimated 2,000 harbor seals resided in Oregon

waters in the 1920s, but about 10,100 were found in 1992. Washington’s population was

estimated to be 34,134 in 1993 and California’s over 30,000 in 1994.

Generally, harbor seals do not feed on salmonids as frequently as California sea lions.

In Puget Sound, harbor seals feed primarily on Pacific hake (Merluccius productus), Pacific

tomcod (Microgadus proximus), walleye pollock (Theragra chalcogramma), flatfish, Pacific

herring, shiner perch (Cymatogaster aggregata), plainfin midshipman (Porichthys notatus),

and sculpins, with some predation on adult salmonids (steelhead, and pink (O. gorbuscha)

and chinook salmon) in the fall.

In Washington outer coastal estuaries and in Oregon, harbor seals have been found to

feed primarily on eulachon, northern anchovy, flatfish, crustaceans, smelt, and sculpin. The

number of scats containing salmonid remains ranges from 1% to 50%, depending on area,

season, and method of analysis (U.S. Dep. Commer. in prep.). In the Russian River, primary

prey were flatfish, octopus (Octopus spp.), Pacific whiting, hagfish (Eptatretus spp.),

plainfish midshipman, cusk-eels, smelt, Pacific herring, and perch. Harbor seals had a catch

rate (number captured/number of attacks) of only 19%, much less than sea lions (Hanson

1993).

Birds

There are many known avian predators of juvenile salmonids, including cormorants

(Phalacrocorax spp.), terns (Sterna spp.), brown pelicans (Pelecanus occidentalis), sooty

shearwaters (Puffinus grisens), common murre (Uria aalge), mergansers (Mergus spp.), gulls

(Larus spp.), belted kingfisher (Megaceryle alcyon), grebes, loons (Gavia spp.), and herons.

Avian predators of adult salmonids include bald eagles (Haliaeetus leucocephalus) and

osprey (Pandion haliaetus).
151

Figure 1. Estimated number of harbor seals (Phoca vitulina) residing in the Columbia River

estuary during May/June. (Data from Robin Brown, Oregon Dep. Fish Wildl.,

7118 NE Vandenberg Ave., Corvallis, OR 97330.)
152

Two species, sooty shearwater and common murre, reside primarily outside estuaries

but eat a considerable number of baitfish and some juvenile salmonids (fish that are often

similar in size). In the 1970s, the sooty shearwater population residing during the fall off

Oregon was estimated to be over 2 million and consumed about 27.2 million kg of prey

(mostly squid and anchovy) (Wiens and Scott 1975). The common murre population along

the Oregon coast is estimated to be about 700,000 birds (R. Lowe, U.S. Fish and Wildlife

Service, Newport, OR, pers. commun.). The Oregon Institute of Marine Biology (1982)

estimated that common murres consumed 60,000 smolts per day off Coos Bay. These birds

concentrated their feeding on recently released hatchery salmonids at the mouth of the bay.

Cormorants

Cormorants are known to consume large numbers of migrating Atlantic salmon

(Salmo salar) smolts (Kennedy and Greer 1988), significantly affecting local fish abundance

(Birt et al. 1987). The double-crested cormorant (Phalacrocorax auritus) population off the

Pacific coast has increased dramatically over the last decade (Table 2) and is estimated at

48,980 nesting pairs. Large population increases have been observed in British Columbia

(1,560%) and Oregon (632%) since 1950 and 1979, respectively (Table 2). However, no data

are presently available indicating that this species is concentrating its feeding on salmonid

smolts and affecting any specific salmon runs.

Caspian terns

The Pacific Coast population of Caspian terns (Sterna caspia) increased 70% from

1960 to 1981 (Gill and Mewaldt 1983) and is probably still increasing. They are known to eat

shiner perch, sculpins, coho (O. kisutch) and chum salmon (O. keta), northern anchovy,

smelt, rainbow trout (O. mykiss), and jacksmelt (Atherinopsis californiensis). Caspian terns

inhabit northwestern estuaries from April to August, when adults typically arrive at northwest

estuaries in April from southern U.S. Pacific Coast or Central America.

Presently, one of the largest nesting colonies of Caspian terns (about 3,000 nesting

pairs) on the West Coast is on Rice Island in the upper Columbia River estuary, an island

made from dredged material. This colony became established after 1980, apparently as a

result of successful breeding and immigration from other areas. Although there are no

Caspian tern food habit data available from this colony, research by Hinton et al. (1992a,

1992b) showed that juvenile salmonids are the dominant fish in this area. Therefore, it is

likely that smolts are consumed by birds from this colony. Assuming a breeding population

of about 6,000 birds, an average fish weight of 10 g, and some standard biological energy

conversions (see Furness and Cooper 1982), I estimate that up to 11 million fish (an

unknown number of which would be salmonids) are potentially consumed each season by

this colony.
153

Table 2. Number and percent increase of breeding double-crested cormorants (Phalacrocorax

auritus) in the Northwest (from Carter et al. 1995).
154

Fishes

Although several freshwater studies have reported substantial salmonid predation in

fresh water by fishes (see Poe et al. 1991), research by McCabe et al. (1983) and others

indicates that large piscivorous fishes that feed on salmonids are not common in most West

Coast estuaries. The primary fish predators in estuaries are probably adult salmonids or

juvenile salmonids which emigrate at older and larger sizes than others. This would include

cutthroat trout (O. clarki) or steelhead smolts preying on chum or pink salmon smolts.

Outside estuaries, many large piscivorous fish populations reside just offshore and

may consume large numbers of smolts. These fishes include Pacific hake, Pacific mackeral

(Scomber japonicus), lingcod (Ophiodon elongatus), spiny dogfish, various rockfish, and

lamprey (Beamish et al. 1992, Pearcy 1992, Beamish and Neville 1995).

Competition

Inter- and intraspecific competition in estuaries is not well documented. Research on

the feeding habits of juvenile salmonids in Northwest estuaries indicates a high diet overlap

between different species (different salmonids and nonsalmonids) and between hatchery and

wild salmonids. However, there are no conclusive data indicating that competition is

occurring (Myers 1980, McCabe et al. 1983, Fisher and Pearcy in prep.). Information on

salmonid growth rates and prey availability during different years, with and without hatchery

influences, would be valuable.

Increased competition may result from the introduction of exotic species which can

alter estuarine food webs. Numerous vertebrate and invertebrate species have been

introduced into West Coast estuaries. San Francisco Bay in particular has an invertebrate

fauna that is now dominated by exotic species that have altered the bay’s food web. For

example, the Asian clam, Potamocorbula amurensis, has reduced abundances of both

phytoplankton and copepod populations (Kimmerer et al. 1994). The recent introduction of

the freshwater Asian shrimp, Exopalaemon modestus, into the Columbia River (personal

observation) could impact salmonid resources. If E. modestus becomes abundant and preys

on and reduces the abundance of the Corophium spp. amphipods (the primary prey for

juvenile salmonids), smolt growth and survival could be reduced. In general, exotic species

can impact salmonid runs if they displace native populations but do not replace them as

important salmonid prey.

American shad (Alosa sapidissima) were introduced along the West Coast in 1871,

1885, and 1886 (Craig and Hacker 1940) and have been identified as a potential estuarine

competitor to salmonids. The largest shad run on the West Coast is in the Columbia River,

which reached a peak of 4 million in 1990, declining to 2 million in 1994 (Fig. 2) (ODFW

and WDFW 1995). Although the potential for competition between shad and salmonids

exists, the migrations in estuaries do not coincide. Adult shad migrate into estuaries primarily
155

Figure 2. Estimated run size of American shad (Alosa sapidissima) in the Columbia River,

1938-94 (from ODFW and WDFW 1995).
156

in June-July and are not actively feeding. Juvenile shad migrate through the estuary during

September-October when most juvenile salmonids have left estuaries.

Conclusions

Estuarine populations of many marine mammals and birds are increasing. These

predators may eat a substantial number of salmonids, depending on location, timing, and

salmonid and alternative prey abundance. Data on the feeding habits of these predators are

critically needed.

Documentation of competition for food in estuaries is very limited. Given the status

of many wild salmonid populations, research is needed to identify possible hatchery vs. wild

smolt interactions in estuaries.

Introductions of exotic species threaten estuarine food webs. Since most exotic

species are introduced by large ship ballast water, legislation forcing ships to off-load, treat,

or exchange ballast water at sea, would reduce the risk of exotic species introductions.

Citations

Barlow, J., R. L. Brownell, Jr., D. P. DeMaster, K. A. Forney, M. S. Lowry, S. Osmek, T. J.

Ragen, R. R. Reeves, and R. J. Small. 1995. U.S. Pacific marine mammal stock

assessments. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-SWFSC-219, 162 p.

Beamish, R. J., and C-E. M. Neville. 1995. Pacific salmon and Pacific herring mortalities in

the Fraser River plume caused by river lamprey (Lampetra ayresi). Can. J. Fish.

Aquat. Sci. 52:644-650.

Beamish, R. J., B. L. Thomson, and G. A. McFarlane. 1992. Spiny dogfish predation on

chinook and coho salmon and the potential effects on hatchery-produced salmon.

Trans. Am. Fish. Soc. 121(4):444-455.

Birt, V. L., T. P. Birt, D. Goulet, D. K. Cairns, and W. A. Montevicche. 1987. Ashmole’s

halo: Direct evidence for prey depletion by a seabird. Mar. Ecol. Prog. Ser. 40:205-

208.

Carter, H. R., A. L. Sowls, M. S. Rodway, U. W. Wilson, R. W. Lowe, G. J. McChesney, F.

Gress, and D. W. Anderson. 1995. Population size, trends, and conservation problems

of the double-crested cormorant on the Pacific Coast of North America. Colonial

Waterbirds 18(Spec. Publ. 1):189-215.
157

Craig, J. A., and R. L. Hacker. 1940. The history and development of the fisheries of the

Columbia River. Fish. Bull., U.S. 32:133-216.

Fisher, J. P., and W. G. Pearcy. In prep. Food habits of juvenile native and hatchery chinook

salmon in Coos Bay, Oregon. Oregon State Univ., Corvallis.

Furness, R. W., and J. Cooper. 1982. Interactions between breeding seabird and pelagic fish

populations in the southern Benguela region. Mar. Ecol. Prog. Ser. 8:243-250.

Gill, R. E., Jr., and L. R. Mewaldt. 1983. Pacific Coast Caspian terns: Dynamics of an

expanding population. The Auk 100:369-381.

Hanson, L. C. 1993. The foraging ecology of harbor seals, Phoca vitulina, and California sea

lions, Zalophus californianus, at the mouths of the Russian River, California. M.A.

Thesis, Sonoma State Univ., Rohnert Park, CA, 70 p.

Harmon, J. R., K. L. Thomas, K. W. McIntyre, and N. N. Paasch. 1994. Prevalence of

marine-mammal tooth and claw abrasions on adult anadromous salmonids returning

to the Snake River. N. Am. J. Fish. Manage. 14:661-663.

Hinton, S. A., R. L. Emmett, and G. T. McCabe, Jr. 1992a. Fishes, shrimp, benthic

invertebrates, and sediment characteristics in intertidal and subtidal habitats at Rice

Island and Miller Sands, Columbia River Estuary. Report to U.S. Army Corps of

Engineers, Contract E96910025, 53 p. (Available from Northwest Fisheries Science

Center, 2725 Montlake Blvd. E., Seattle, WA 98112-2097.)

Hinton, S. A., R. L. Emmett, and G. T. McCabe, Jr. 1992b. Benthic invertebrate and

sediment characteristics in subtidal habitat at Rice Island, Columbia River estuary,

December 1991 and March 1992. Report to U.S. Army Corps of Engineers, Contract

E96920018, 22 p. (Available from Northwest Fisheries Science Center, 2725

Montlake Blvd. E., Seattle, WA 98112-2097.)

Kennedy, G. J., and J. E. Greer. 1988. Predation by cormorants, Phalacrocorax carbo (L.),

on the salmonid populations of an Irish river, Northern Ireland, UK. Aquacult. Fish.

Manage. 19:159-170.

Kimmerer, W. J., E. Gartside, and J. J. Orsi. 1994. Predation by an introduced clam as the

likely cause of substantial declines in zooplankton of San Francisco Bay. Mar. Ecol.

Prog. Ser. 113:81-93.

McCabe, G. T., Jr., W. D. Muir, R. L. Emmett, and J. T. Durkin. 1983. Interrelationships

between juvenile salmonids and nonsalmonid fish in the Columbia River estuary.

Fish. Bull., U.S. 81:815-826.
158

Myers, K. W. W. 1980. An investigation of the utilization of four study areas in Yaquina

Bay, Oregon by hatchery and wild juvenile salmonids. M.S. Thesis, Oregon State

Univ., Corvallis, OR, 234 p.

Oregon Department of Fish and Wildlife (ODFW) and Washington Department of Fish and

Wildlife (WDFW). 1995. Status report: Columbia River fish runs and fisheries, 1938-

94. Oregon Dep. Fish Wildl., Portland, OR and Wash. Dep. Fish. Wildl., Olympia,

WA, 291 p.

Oregon Institute of Marine Biology. 1982. The impact of seabird feeding on coho smolt

survival. Unpubl. research proposal by Univ. Oregon Inst. Mar. Biol., Charleston, 9 p.

(Available from Oregon Institute of Marine Biology, P.O. Box 5389, Charleston, OR

97420.)

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Washington Sea Grant,

Seattle, 179 p. (Available from Department of Oceanography and Atmospheric

Sciences, Bert 114, Oregon State University, Corvallis, OR 97330.)

Poe, T. P., H. C. Hansel, S. Vigg, D. E. Palmer, and L. A. Prendergast. 1991. Feeding of

predaceous fishes on out-migrating juvenile salmonids in John Day Reservoir,

Columbia River. Trans. Am. Fish. Soc. 120(4):405-420.

Roffe, T. J., and B. R. Mate. 1984. Abundances and feeding habits of pinnipeds in the Rogue

River, Oregon. J. Wildl. Manage. 48(4):1262-1274.

U.S. Department of Commerce. In prep. Review of information on the impacts of California

sea lions and Pacific harbor seals on salmonids and the coastal ecosystems of

Washington, Oregon, and California. U.S. Dep. Commer., NOAA, Tech. Memo.

NMFS-NWFSC.

Wiens, J. A., and J. M. Scott. 1975. Model estimation of energy flow in Oregon coastal

seabird populations. Condor 77:439-452.
159

CRITERIA FOR EVALUATING THE SURVIVAL VALUE OF

ESTUARIES FOR SALMONIDS

C. D. Levings1 and D. Bouillon2

1

Department of Fisheries and Oceans (DFO)

West Vancouver Laboratory

4160 Marine Drive

West Vancouver, BC, Canada V7V 1N6

2

ESSA Technologies Ltd., Suite 300

1765 W 8th Avenue

Vancouver, BC, Canada V6J 5C6

It is well known that estuaries have been affected by human use of the coastal zone

and in the Northeast Pacific between southwestern British Columbia and California most of

these habitats are either degraded or threatened (Levings 1994a). In the life cycle of a

salmon, the estuary is also the animal’s last “address” where the natural landscape can be

changed by the direct activities of industrial activity or urbanization such as filling and direct

habitat change. After leaving the estuary, the juvenile salmon’s address in the pelagic zone is

susceptible to the biophysical attributes of water quality (temperature and salinity) but not to

water quantity or direct loss of habitat. However, with the possible exception of greenhouse

gases and their effect on global warming, pelagic habitats cannot be “managed.” Since

decisions about estuarine salmon habitat have significant societal impacts in addition to those

dealing with salmonid productivity, it is important to verify the role of estuaries in salmon

survival.

We describe a scheme developed by Fox (1991) which may help in the latter exercise,

and in the process we briefly review some of the literature on salmon ecology. Fox

recognized that concepts used by epidemiologists to test hypotheses on how diseases were

spread could be applied to cause-effect relationships for pollution problems. By applying the

null hypothesis, scientists are forced to consider how much information must be ignored to

conclude that a causal relationship does not exist. In the present paper, we propose an

extension to the issue of estuarine habitat management for maintenance of salmon

production. Using seven criteria, the object of the scheme is to “draw together all the

disparate threads of evidence and make them into a coherent whole, so that scientifically and

socially defensible regulatory decisions can be made” (Fox 1991). The seven criteria are as

follows: probability, time order or chronological relationship, strength of the association,

specificity, consistency of the association upon replication, predictive performance, and

coherence. Because the scheme is based on the functioning of natural systems, we have

restricted our considerations to wild salmon since it is well known that hatchery reared fish

show very different patterns of estuarine use relative to wild stocks (e.g., Myers 1978,

Levings et al. 1986).
160

Probability

Rice (1993) used the kernel estimator methodology to determine cumulative

probability ogives for the abundance of several fish species including Atlantic cod (Gadus

morhua) and Atlantic salmon (Salmo salar). We have tested this nonparametric technique

with beach-seine data for juvenile hatchery chinook salmon (Oncorhynchus tshawytscha) at

the Campbell River estuary. We used salinity as a parameter and found the method shows

some promise to give predictions about the salinity adaptations of young salmon (Fig. 1). The

preliminary results showed that while there is 80% probability of catch per unit of effort

(CPUE) of 15 at 0.5‰, the probability of this CPUE at a higher salinity (5‰) is only about

10%. This indicates that hatchery chinook were more abundant in the lower salinity habitats

of the estuary, probably in response to osmoregulatory requirements.

Time Order or Chronological Relationship

Fry from ocean-type chinook, chum (O. keta), and certain sockeye (O. nerka) salmon

stocks undergo a rearing migration from freshwater habitats in the upper estuary to brackish

areas of intermediate salinity and finally into marine habitats as they complete smoltification

(Levy and Northcote 1982, Levings et al. 1986, Birtwell et al. 1987). The residence time of

the fish in particular salinity regimes is attuned to the species’ development of

osmoregulatory ability at certain sizes and ages. The movement through the estuary over the

spring to summer period follows an adaptive chronology which bears out the survival value

of estuarine residency.

Strength of the Association

It is a qualitative, but well-documented, observation that juvenile ocean-type chinook

salmon appear to be strongly linked to estuarine habitats since they reside in these habitats

for 1 to 2 months (e.g., Healey 1982, Levy and Northcote 1982). Many estuaries almost

totally drain with falling tides and are characterized by strong currents (e.g., Campbell River

estuary; > one m•s-1, Ages et al. 1990) and shallow brackish layers which a priori might lead

to flushing the fry out of these habitats. However, they are adapted to remain and rear before

smoltification and departure to the open sea.

Specificity

Specificity refers to the precision of the association between a cause (X) and an effect

(Y). Does X lead only to Y (specificity of effect) or does only X lead to Y (specificity of

cause) (Fox, 1991)? In our context the question could be reformulated to ask if the loss (X) of

an estuary in the life history of a particular wild salmon stock leads to decreased survival (Y)
161
162

(specific of effect). It is obvious that a very elaborate and detailed research program would be

needed to identify the second part of the proposal, namely specificity of cause.

The initial observations of Reimers (1973) in Oregon estuaries concerning the relative

survival of several chinook salmon life history types that showed differences in estuarine use

led to several major research programs in estuaries of the Northeast Pacific. This question

was asked in a series of habitat release experiments with juvenile chinook salmon at the

Campbell River estuary, as described in Levings (1984), Macdonald et al. (1988), and

Levings et al. (1989). Releases of specially marked fish were made to river, estuary,

transition, and marine habitats in 1983, 1984, and 1985. About 35,000 fish were released into

the four habitats each year. Results showed that survival, to catch and escapement, of the fish

that transitted the estuary was higher than for those that did not (Table 1). A similar result

was found with steelhead (O. mykiss) reared and released in the estuary of the Keogh River

on Vancouver Island. Releases directly to ocean habitats also showed lower survival in the

latter experiments. However, there were numerous complications to the interpretations of the

results of both the chinook salmon experiments (Levings et al. 1989) and the steelhead

releases (Ward and Slaney 1990), including size effects and differences in temperature and

ocean conditions that the three brood years were exposed to.

Consistency of the Association upon Replication

Levings (1984) summarized data to show that densities of juvenile salmon in

estuaries were within a relatively narrow range, which might suggest some consistency in the

number of juvenile salmon that the estuaries could support. To further assess the use of this

concept to ecological data on the importance of estuaries to juvenile salmon, we assembled

data on instantaneous growth in weight for chinook and chum salmon in six estuaries off the

Strait of Georgia (Fig. 2). The six estuaries might be considered replicates of the habitats and

ecosystems we are concerned with. Instantaneous growth rates for chinook salmon ranged

between 0.02% and 0.04% and for chum salmon between 0.01% and 0.03%. These data show

that growth in the various estuaries did not vary randomly over the landscapes sampled.

These findings suggest that these wild salmonids are adapted to estuarine rearing and imply

that growth was not being impaired, relative to comparisons possible with this particular data

set.

Predictive Performance

In a quantitative or statistical sense (as per Fox 1991), predictive performance may be

interpreted as the size of effect produced by the presumptive cause. For example, Morley et

al. (1996) used response surface analysis to investigate relationships between size and time of

release of hatchery reared chinook salmon. Experiments were conducted in 1982 and 1983,

with releases in May, June, and July. Results showed that fish released in May had best

survival and that time effects were apparently more important than those for size.
163

Table 1. Total number of tags recovered from experimental releases of juvenile chinook

salmon into four habitats at Campbell River estuary (unpublished DFO data

subject to verification, compiled to 1991).
164
165

Coherence

Sibert and Kask (1978) analyzed the correlations between the diet of juvenile chinook

salmon at the Nanaimo, Cowichan, Fraser, and Campbell River estuaries, as measured by

conventional taxonomic methods. They found significant correlations in a minority of cases,

indicating low coherence in fish diets at the four estuaries. It is clear that factors such as prey

size, color, behavior, and perhaps nutrition may be important factors influencing prey

selection from the suite of available organisms (Levings 1994b, Higgs et al. 1995). However,

coherence in food webs may also be assessed by methods such as radiotracer experiments or

stable isotope concentrations at various trophic levels. Over the past two decades there have

been numerous papers which show that juvenile salmonids are linked to the detritus-based

food webs of estuaries (e.g., Sibert et al. 1977, Simenstad and Wissmar 1985, Levings

1994c). These reports support the idea that heterotrophy and detrital production are

responsible for coherent energy flow patterns in Northeast Pacific estuaries.

Conclusions

Several experiments have investigated the causal relationship between estuaries and

survival of juvenile salmonids since the 1983 Workshop (Levings 1984), but it is clear that

much research has yet to be done in this particular habitat. The existing data, tested using a

causal inference scheme, supports the rejection of the null hypothesis that estuaries are not

important for salmon survival. Salmon ecologists from outside the Northeast Pacific, notably

Thorpe (1994), agree with this conclusion based on evolutionary considerations. Thorpe

concluded that wild pink (O. gorbuscha), chum, some sockeye, and ocean-type chinook

salmon are adapted to rear in estuaries and thus their natural habitat characteristics have

survival value relative to fresh water. Evidence for the significance of smolt rearing in

estuaries by coho, most sockeye, stream-type chinook, masu (O. masou), and Atlantic

salmon, cutthroat and brown trout (Salmo trutta), and steelhead is more equivocal.

One of the problems of resolving the question of the importance of estuaries for

salmon in the Northeast Pacific is the fact that most of the data are from south of 50°N

latitude where stocks are dominated by hatchery fish and habitats are disrupted. Thus many

of the data are not applicable to more northern areas where a major concerted effort must be

maintained to preserve wild stocks and natural habitat. In some designated watershed-estuary

ecosystems, production of salmon may have to be sacrificed to conservation if we are to

appreciate and understand the role of estuaries in salmon ecology (Levings 1993).

Acknowledgments

Thanks are owed to Derek Nishimura for assistance with computing probability

density functions. Some of the work reported herein was supported by the DFO Habitat

Action Plan, Environmental Analysis component.
166

Citations

Ages, A. B., F. A. Dobbs, and C. D. McAllister. 1990. The salinity intrusion in the Campbell

River estuary: Salinity, temperature and current observations, 1984-1986. Can. Data

Rep. Hydrog. Ocean Sci. 83(1):1-243 and 83(2):1-191.

Birtwell, I. K., M. D. Nassichuk, and H. Buene. 1987. Underyearling sockeye salmon

(Oncorhynchus nerka) in the estuary of the Fraser River. In H. D. L. Smith, L.

Margolis and C. C. Wood (editors), Sockeye salmon (Oncorhynchus nerka)

population biology and future management. Can. Spec. Publ. Fish. Aquat. Sci. 96:25-

35.

Bouillon, D. 1996. A comparison of growth and bioenergetic consumption of juvenile

salmon in several estuaries of the Strait of Georgia, 68 p. (Available from DFO, West

Vancouver Laboratory, West Vancouver, BC, Canada.)

Fox, G. A. 1991. Practical causal inference for ecoepidemiologists. J. Toxicol. Environ.

Health 33:359-373.

Healey, M. C. 1982. Juvenile Pacific salmon in estuaries: The life support system. In V. S.

Kennedy (editor), Estuarine comparisons, p. 315-342. Academic Press, New York.

Higgs, D. A., J. S. Macdonald, C. D. Levings, and B. Dosanjh. 1995. Nutrition and feeding

habits of Pacific salmon (Oncorhynchus spp.) in relation to life history stage. In R.

Brett, W.C. Clarke, K. Groot, and L. Margolis (editors), Physiological ecology of

Pacific salmon, p. 161 to 315. Univer. B.C. Press, Vancouver, B.C.

Levings, C. D. 1984. Commentary: Progress in attempts to test the null hypothesis that

juvenile salmonids aren’t dependent on estuaries. In W. G. Pearcy (editor), The

influence of ocean conditions on the production of salmonids in the North Pacific,

p. 287-296. Oreg. State Univ., Sea Grant Coll. Prog. ORESU-W-83-001.

Levings, C. D. 1993. Requirements for genetic data on adaptations to environment and

habitats of salmonids. In J. G. Cloud and G. H. Thorgaard (editors), Proceedings of

NATO Advanced Study Institute: Genetic Conservation of Salmonid Fishes,

Moscow, Idaho, June 23-29, 1992, p. 49-65. Plenum Press, New York.

Levings, C. D. 1994a. Science and management needed to maintain salmon production in

estuaries of the Northeast Pacific. In K. Dyer and R. J. Orth (editors), Proceedings

Joint Symposium of Estuarine Research Federation and Estuarine and Coastal

Sciences Association, September 14-18 1992, Plymouth, England, p. 417-421. Olsen

and Olsen, Denmark.
167

Levings, C. D. 1994b. Feeding behaviour of juvenile salmon and significance of habitat

during estuary and early sea phase. Nordic J. Freshw. Res. 69:7-16.

Levings, C. D. 1994c. Life on the edge: Structural and functional aspects of chinook and

coho rearing habitats on the margins of the lower Fraser River. In Salmon ecosystem

restoration: myth and reality, Proceedings of 1994 Northeast Pacific Chinook and

Coho Salmon Workshop, Oregon Chapter, American Fisheries Society, Corvallis,

OR, p. 139-147.

Levings, C. D., McAllister, C. D., and B. D. Chang. 1986. Differential use of the Campbell

River estuary, British Columbia, by wild and hatchery reared juvenile chinook

salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci. 43:1386-1397.

Levings, C. D., C. D. McAllister, J. S. Macdonald, T. J. Brown, M. S. Kotyk, and B. A.

Kask. 1989. Chinook salmon (Oncorhynchus tshawytscha) and estuarine habitat: A

transfer experiment can help evaluate estuary dependency. Can. Spec. Publ. Fish.

Aquat. Sci. 105:116-122.

Levy, D. A., and T. G. Northcote. 1982. Juvenile salmon residency in a marsh area of the

Fraser River estuary. Can. J. Fish. Aquat. Sci. 39:270-276.

Macdonald, J. S., C. D. Levings, C. D. McAllister, U. H. M. Fagerlund, and J. R. McBride.

1988. A field experiment to test the importance of estuaries for chinook salmon

(Oncorhynchus tshawytscha) survival: short term results. Can. J. Fish. Aquat. Sci.

45:1366-1377.

Morley, R. B., A. Y. Federenko, H. T. Bilton, and S. J. Lehmann. 1966. The effects of time

and size at release on returns at maturity of chinook salmon from Quinsam Hatchery,

B.C., 1982 and 1983 releases. Can. Tech. Rep. Fish. Aquat. Sci. No. 2105. 62 p.

Myers, K. W. 1978. Comparative analysis of stomach contents of cultured and wild juvenile

salmonids in Yaquina Bay, Oregon. In S. J. Lipovsky and C. A. Simenstad (editors),

Fish food habits studies, p. 155-162. Proceedings of the Second Pacific Northwest

Technical Workshop, October 10-13, 1978, Washington Sea Grant, Univ.

Washington, Seattle.

Reimers, P. E. 1973. The length of residence of juvenile fall chinook salmon in Sixes River,

Oregon. Res. Briefs Fish. Comm. Oregon 4(2):1-43.

Rice, J. R. 1993. Forecasting abundance from habitat measures using non-parametric density

estimate methods. Can. J. Fish. Aquat. Sci. 50:1690-1698.
168

Sibert, J. R., T. J. Brown, M. C. Healey, B. A. Kask, and R. J. Naiman. 1977. Detritus-based

food webs: exploitation by juvenile chum salmon (Oncorhynchus keta). Science

196:649-650.

Sibert, J., and B. A. Kask. 1978. Do fish have diets? In B. G. Shepherd and R. M. J. Ginetz

(rapporteurs), Proceedings of the 1977 Northeast Pacific Chinook and Coho Salmon

Workshop, p. 48-56. Fisheries and Marine Service Tech. Rep. 759.

Simenstad, C. A., and R. C. Wissmar. 1985. δ 13C evidence of the origins of organic carbon

in estuarine and nearshore food webs. Marine Ecology (Progress Series) 22:141-152.

Thorpe, J. E. 1994. Salmonid fishes and the estuarine environment. Estuaries 17(1A):76-93.

Ward, B. R., and P. A. Slaney. 1990. Returns of pen-reared steelhead from riverine,

estuarine, and marine releases. Trans. Am. Fish. Soc. 119:492-299.
169

ESTUARINE POLLUTION AND JUVENILE SALMON HEALTH:

POTENTIAL IMPACT ON SURVIVAL

E. Casillas, B. B. McCain, M. Arkoosh, and J. E. Stein

Environmental Conservation Division

Northwest Fisheries Science Center

2725 Montlake Blvd. E.

Seattle, WA 98112-2097

The marked declines in several Pacific Northwest salmon stocks are attributed to the

cumulative effects of natural and anthropogenic factors. Although the relative contributions

of these factors to changes in individual runs are not well understood, human impacts on the

environment have contributed significantly to stock declines in many river systems. Human

impacts on various life history stages of salmon in freshwater habitats include certain forest

and agricultural practices, dams, water diversions, and urbanization. The addition of

hatcheries to mitigate the human-induced losses of habitat has also been recently recognized

as another potentially important factor affecting the survival of wild stocks of salmon. In the

ocean, an important anthropogenic factor is harvesting, whereas natural environmental

factors, including climatic changes, reduced food availability, and predation are the other

forces thought to influence survival of juvenile and subadult salmon.

Estuaries serve as the natural linkage for salmon migrating between freshwater and

ocean environments, providing the necessary habitat for their transition. Because of the

urbanization of many coastal regions, estuaries located near urban centers are known to

receive both point and nonpoint inputs of chemical contaminants from municipal and

industrial activities. Many of the chemicals from these sources are known to accumulate in

estuarine sediments (McCain et al. 1988), and a large number of these chemicals are

bioaccumulated by sediment-dwelling organisms, including amphipods and copepods, which

are important prey organisms for downstream migrant juveniles of certain salmonid species

(McCain et al. 1990). As a result, pollution in urban estuaries is one anthropogenic factor that

may influence the survival of juvenile salmon, whether directly in the estuary or

subsequently in the nearshore ocean.

Recent studies in several urban estuaries, including San Francisco Bay, Elliott Bay

and Commencement Bay in Puget Sound, and the Fraser River estuary in Vancouver, British

Columbia, have shown that juvenile fall chinook salmon (Oncorhynchus tshawytscha)

accumulate significant concentrations of chemical contaminants during their relatively short

residence time. In studies conducted in urban estuaries in Puget Sound by our laboratory, we

found evidence of exposure to high levels of polycyclic aromatic hydrocarbons (PAHs) and

polychlorinated biphenyls (PCBs) (McCain et al. 1990, Stein et al. 1995). For example, we

consistently found significantly elevated concentrations of fluorescent aromatic compounds

(FACs) in bile of juvenile salmon from urbanized estuaries compared to concentrations in
170

fish from nonurban estuaries (Fig. 1). Because fish extensively metabolize PAHs, the parent

compounds do not accumulate in tissues but are found in the bile as metabolites (Varanasi et

al. 1989). Measurement of these metabolites, quantified as FACs, provides an estimate of

exposure of fish to PAHs (Krahn et al. 1986). Concentrations of PCBs in the liver of juvenile

salmon were also significantly higher in fish from the urban estuaries compared to fish from

hatcheries and nonurban estuaries. No significant differences in tissue levels of selected toxic

metals were found in this study.

We have also demonstrated in field and laboratory studies that juvenile salmon from

polluted environments exhibit abnormalities ranging from subcellular effects to changes in

immune function and growth. In many cases the effects alter physiological processes, such

that the potential for survival is reduced. As an example, chemically induced

immunosuppression and the subsequent increased susceptibility to disease represent a serious

problem to exposed animals. Immune dysfunction in mammals and fish has been recognized

as a sublethal effect of chemical contaminant exposure affecting both cellular and humoral

aspects of the immune system (McLeay and Gordon 1977, Dean et al. 1986, Arkoosh and

Kaattari 1987, Rice and Weeks 1989, Thuvander 1989).

In our studies with juvenile salmon, immunocompetence was evaluated by analyzing

the functional ability of leukocytes to produce an in vitro primary and secondary plaqueforming cell (PFC) response to a foreign antigen. This has been shown to be a very sensitive

approach to evaluating the long-term chronic effects of exposure to chemical contaminants

for short time periods (Arkoosh and Kattari 1987). We showed that leukocytes of juvenile

salmon collected from hatcheries and from a nonurban estuary were able to generate a

significantly higher secondary PFC response to a foreign antigen than that produced during

the primary PFC response, which is the normal and expected response (Arkoosh et al. 1991).

However, an enhanced secondary PFC response did not occur with leukocytes of juvenile

salmon exposed to pollution from an urban estuary (Arkoosh et al. 1991) (Fig. 2).

Both PAHs and PCBs are known to induce immunoaltering effects in mammals

(Ward et al. 1985, Dean et al. 1990), suggesting that PCBs or PAHs or both may be

responsible for a suppressed PFC response to an antigen in juvenile salmon from the

contaminated urban estuary. This hypothesis was supported by the results of our recent

laboratory studies (Arkoosh et al. 1994). Juvenile chinook salmon were administered

sublethal doses of PAHs and PCBs. The exposed fish exhibited suppression of their

secondary PFC responses. Thus, an impaired secondary PFC response has been demonstrated

in both field and laboratory studies, supporting the putative causal relationship between

impaired immunity and chemical contaminant exposure in juvenile fall chinook salmon from

polluted urban estuaries.

These physiological effects have recently been linked to increased susceptibility to

disease. Infectious diseases are commonly suspected of contributing to mortality of juvenile

salmon in estuarine and nearshore environments (Elliott et al. 1995). We collected juvenile

fall chinook salmon from urban and nonurban estuaries, and from the respective releasing

hatcheries, and exposed them in the laboratory to the marine pathogen Vibrio anguillarum.
171

Figure 1. Biliary fluorescent aromatic compounds (FACs) (ng BaP (benzo[a]pyrene)

equivalents/mg bile protein) in juvenile salmon from hatcheries, a nonurban

estuary (the Nisqually River estuary), and an urban estuary (the Duwamish

Waterway) sampled in Puget Sound, Washington in 1990. The bars represent the

mean ± standard error (n=3 to 8). Each sample represents a composite of material

from 60 fish (adapted from Stein et al. 1995).
172

Figure 2. The number of primary and secondary plaque-forming cells/culture of juvenile

chinook salmon from the hatcheries, a nonurban estuary (the Niqually River

estuary), and an urban estuary (the Duwamish Waterway) in response to an

antigen. The bars represent the mean ± standard deviation (adapted from Arkoosh

et al. 1991).
173

We found that juvenile chinook salmon from the contaminated estuary were more susceptible

to V. anguillarum-induced mortality than fish from the corresponding hatchery (Fig. 3). In

contrast, juvenile fall chinook salmon from the nonurban estuary were not more susceptible

to V. anguillarum-induced mortality than the fish from the corresponding hatchery. The

results of these initial disease challenges indicate that, in juvenile chinook salmon from an

urban estuary, contaminant-associated immunodysfunction appears to lead to increased

susceptibility to pathogenesis by a virulent marine bacterium. Similar findings were reported

by Servizi et al. (1993) for outmigrating juvenile chinook salmon in the Fraser River estuary.

In their laboratory based study evaluating the toxic effects of bleached kraft mill effluents,

they observed an increased prevalence of bacterial kidney disease (a chronic bacterial

infection of salmonids) in juveniles following a 212-day study simulating exposure to

pollutants found in the Fraser River.

Immunosuppression and the subsequent increased susceptibility to disease are not the

only potential deadly effects of exposure to chemical contaminants in urban estuaries. Effects

on neuronal function and subsequently on behavior have been reported in juvenile salmonids

exposed to 2-(thio-cyanomethylthio) benzothiazole (TCMTB), an antisapstain fungicide used

to protect freshly cut lumber. Exposure of juvenile chinook salmon to TCMTB at levels

comparable to exposures occurring in the Fraser River estuary increased susceptibility to

predation by a natural marine predator, yellowtail rockfish (Sebastes flavidus) (Kruzynski

and Birtwell 1994). Although the mechanisms and the linkages between exposure and

biological effects are not fully delineated, the performance-based assessment on survival

potential is ecologically relevant. The implication to survival of juvenile salmon in an

environment at times of high predator densities is indicated by the study of Beamish and

Neville (1995) showing that the potential impact of predation by lamprey on juvenile chinook

salmon in the Fraser River estuary plume may reduce by a large percentage (nearly 50%) the

recruitment potential of hatchery fish to harvest. Thus, increasing the chemical contaminant

burden in urban estuaries may have even greater implications to the survival of a stock

already depressed.

The findings presented here strongly indicate that, in addition to the myriad

anthropogenic factors that can affect the survival of outmigrating juvenile fall chinook

salmon in fresh water, the biological effects of chemical contaminants on these fish during

their residency in certain urban estuaries can also potentially lead to reduced survival.

Concomitant with the increased chemical exposure, juvenile chinook salmon inhabiting

certain urban estuaries exhibit evidence of impairment of physiological processes such as

immune system alterations, impaired growth (not described here), and behavioral changes.

The assessment of the long-term effects of physiological changes induced by chemical

pollution in urban estuaries on selected salmon stocks can be placed into context by using

performance-based evaluations of effects at the level of the organism (Fig. 4). Overall, the

findings from these recent studies provide evidence of linkage between the presence of

elevated levels of complex mixtures of chemical contaminants in polluted estuaries and

effects on health and survival of juvenile chinook salmon. Additional research is clearly

needed to address the large gaps in understanding concerning the effects of oceanic factors on
174

Figure 3. Percent cumulative mortality of juvenile chinook salmon from hatcheries and

estuaries of a nonurban and urban river system from Puget Sound, Washington,

after 4 days exposure to Vibrio anguillarum (adapted from Arkoosh et al. in

preparation).
175

Figure 4. Conceptual model of relationships between toxic chemical exposure and

population-level impacts in juvenile chinook salmon. Performance-based

assessments, such as plaque-forming cell response (immune function), growth rate,

disease challenge, and predator avoidance, are used to link physiological and

organismal effects to potential population-level impacts.
176

salmon survival. However, this recent evidence suggesting that outmigrant juvenile fall

chinook salmon are experiencing sublethal effects from toxic chemical exposure during their

residence in urbanized estuaries indicates the need to further investigate estuarine pollution

as a contributing factor to declines in salmon stocks from urbanized watersheds.

Citations

Arkoosh, M. R., E. Casillas, E. Clemons, B. B. McCain, and U. Varanasi. 1991. Suppression

of immunological memory in juvenile chinook salmon (Oncorhynchus tshawytscha)

from an urban estuary. Fish & Shellfish Immunol. 1:261-277.

Arkoosh, M. R., E. Casillas, P. Huffman, E. Clemons, J. Evered, J. E. Stein, and U. Varanasi.

In prep. Increased susceptibility of juvenile chinook salmon (Oncorhynchus

tshawytscha) from a contaminated estuary to the pathogen Vibrio anguillarum.

Arkoosh, M. R., E. Clemons, M. Myers, and E. Casillas. 1994. Suppression of B-cell

mediated immunity in juvenile chinook salmon (Oncorhynchus tshawytscha) after

exposure to either a polycyclic aromatic hydrocarbon or to polychlorinated biphenyls.

Immunopharmacol. Immunotoxicol. 16:293-314.

Arkoosh, M. R., and S. L. Kaattari. 1987. Effect of early aflatoxin B1 exposure on in vivo and

in vitro antibody responses in rainbow trout, Salmo gairdneri. J. Fish Biol.

31(Supplement A):19-22.

Beamish, R. J., and C-E. M. Neville. 1995. Pacific salmon and Pacific herring mortalities in

the Fraser River plume caused by river lamprey (Lampetra ayresi). Can. J. Fish.

Aquat. Sci. 52:644-650.

Dean, J. H., J. B. Cornacoff, and M. I. Luster. 1990. Toxicity to the immune system:

A review. In J. W. Hadden and A. Szentivanyi (editors), Immunopharmacology

reviews, p. 377-410. Plenum Press, New York.

Dean, J. H., M. J. Murray, and E. C. Ward. 1986. Toxic responses of the immune system. In

C. D. Klassen, M. O. Amdur, and J. Doull (editors), Casarett and Doull’s Toxicology.

The basic science of poisons, p. 245-285. Macmillan, New York.

Elliott, D. G., R. J. Pascho, and A. N. Palmisano. 1995. Brood stock segregation for the

control of bacterial kidney disease can affect mortality of progeny chinook salmon

(Oncorhynchus tshawytscha) in seawater. Aquaculture 132:133-144.
177

Krahn, M. M., L. D. Rhodes, M. S. Myers, L. K. Moore, W. D. MacLeod, Jr., and D. C.

Malins. 1986. Associations between metabolites of aromatic compounds in bile and

the occurrence of hepatic lesions in English sole (Parophrys vetulus) from Puget

Sound, Washington. Arch. Environ. Contam. Toxicol. 15:61-67

Kruzynski, G. M., and I. K. Birtwell. 1994. A predation bioassay to quantify the ecological

significance of sublethal responses of juvenile chinook salmon (Oncorhynchus

tshawytscha) to the antisapstain fungicide TCMTB. Can. J. Fish. Aquat. Sci. 51:1780-

1790.

McCain, B. B., D. W. Brown, M. M. Krahn, M. S. Myers, R. C. Clark, Jr., S-L. Chan, and D.

C. Malins. 1988. Marine pollution problems, North American West Coast. Aquat.

Toxicol. 11:143-162.

McCain, B. B., D. C. Malins, M. M. Krahn, D. W. Brown, W. D. Gronlund, L. K. Moore,

and S-L. Chan. 1990. Uptake of aromatic and chlorinated hydrocarbons by juvenile

chinook salmon (Oncorhynchus tshawytscha) in an urban estuary. Arch. Environ.

Contam. Toxicol. 19:10-16.

McLeay, D. J., and M. R. Gordon. 1977. Leucocrit: A simple hematological technique for

measuring acute stress in salmonid fish, including stressful concentrations of pulpmill

effluent. Am. Fish. Soc. Symp. 7:317-322.

Rice, C. D., and B. A. Weeks. 1989. Influence of tributyltin on in vitro activation of oyster

toadfish macrophages. J. Aquat. Anim. Health. 1:62-68.

Servizi, J. A., R. W. Gordon, D. W. Martens, W. L. Lockhart, D. A. Metner, I. H. Rogers, J.

R. McBride, and R. J. Norstrom. 1993. Effects of biotreated bleached kraft mill

effluent on fingerling chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish.

Aquat. Sci. 50:846-857.

Stein, J. E., T. Hom, T. K. Collier, D. W. Brown, and U. Varanasi. 1995. Contaminant

exposure and biochemical effects in outmigrant juvenile chinook salmon from urban

and nonurban estuaries of Puget Sound, Washington. Environ. Toxicol. Chem.

14:1019-1029.

Thuvander, A. 1989. Cadmium exposure of rainbow trout, Salmo gairdneri Richardson:

Effects of immune functions. J. Fish Biol. 35:521-529.

Varanasi, U., J. E. Stein, and M. Nishimoto. 1989. Biotransformation and disposition of

polycyclic aromatic hydrocarbons (PAH) in Fish. In U. Varanasi (editor), Metabolism

of polycyclic aromatic hydrocarbons in the aquatic environment, p. 93-149. CRC

Press, Boca Raton, Florida.
178

Ward, E. C., M. J. Murray, and J. H. Dean. 1985. Immunotoxicity of nonhalogenated

polycyclic aromatic hydrocarbons. In J. H. Dean, M. I. Luster, A. E. Munson, and H.

Amos (editors), Immunotoxicolgy and immunopharmacology, p. 291-303. Raven

Press, New York.
179
180
181

Process and Mechanisms—Nearshore Coastal
182
183

FACTORS INFLUENCING THE MARINE SURVIVAL OF PINK SALMON

IN PRINCE WILLIAM SOUND, ALASKA

Robert T. Cooney and T. Mark Willette

Institute of Marine Science

University of Alaska Fairbanks

Fairbanks, AK 99775-1080

and

Alaska Department of Fish and Game

Cordova, AK 99574

Pink salmon (Oncorhynchus gorbuscha) are the most abundant of the five Pacific

salmon species in Alaska (Rogers 1986). Wild stocks in Prince William Sound have

historically demonstrated negligible odd-even year cycle dominance, although other, longer

term trends are evident since 1960 (Fig. 1). Adult returns of less than 10 million fish per year

increased to nearly 20 million fish in 1979 and for several years following, but returned to

lower production levels in 1986. Since that time, only the returns in 1990, 1991, and 1994

have approached or surpassed 10 million fish. Similar decadal-level production cycling has

been described for salmonids in Alaska (Hare and Francis 1995).

A large ocean-ranching program for pink salmon was initiated in 1977. Growing

hatchery capacity drove increasingly larger releases of juveniles that peaked in 1991 at

616 million fry. Since 1987, hatchery-released rather than wild pink salmon have been the

numerically dominant stock in Prince William Sound. Annual percent marine survivals for

hatchery fry to adults have ranged between 1.0 and 9.8, and average 4.4 (Alaska Department

of Fish and Game, unpublished). Two of the three poorest production years were recent: 1992

and 1993. There is concern that a hatchery program of this size is seriously impacting the

wild production in the region, although direct negative effects have not been demonstrated.

An elaborately phased fishery attempts to separate harvests on wild and hatchery stocks as

the means to protect the wild escapement each year.

Alaska Department of Fish and Game has censused pre-emergent fry populations

since 1962 in index streams in Prince William Sound. These measures generally predict adult

returns and have been used as the principal area forecast tools for wild stocks. When the wild

return per fry density (a proxy for marine survival) is compared with hatchery marine

survivals beginning in 1977, it is apparent that years of good, average, or poor survivals are

phased similarly (Fig. 2). This relationship supports a contention that common marine factors

influence the survival of both populations.
184

Figure 1. Historical adult returns of wild and hatchery released pink salmon in Prince

William Sound, Alaska.
185

Figure 2. Comparisons between wild and hatchery marine survivals for pink salmon in

Prince William Sound, Alaska.
186

The salmon literature suggests that pink salmon run strength is established each year

during early marine residence, perhaps during the first few weeks in the coastal ocean (Parker

1971, Hartt 1980, Healey 1982, Bax 1983, Hargreaves and LeBrasseur 1985). The

mechanism for loss is believed to be predation, and the rate of loss is thought to be modified

by the growth rate of the fry during this critical period. The slowest growing fish probably

experience the highest rates of mortality since they remain at risk longer in the smallest,

presumably weakest, life stages. Temperature and food have been implicated as the major

factors influencing growth rates (Walters et al. 1978, Mortensen 1983, Healey 1991).

Locally, Willette (1985) and Willette and Cooney (1991) found that production levels of odd

and even year southcentral Alaska pink salmon stocks are sensitive to fry-year spring-time

ocean temperatures, and that the odd brood lines are also influenced by ocean temperatures

during the late maturing and adult stages.

Wild juvenile pink salmon in the northern Gulf of Alaska begin emerging into the

nearshore tidally mixed zone in late March. The outmigration from natal habitats is usually

completed by early June (Taylor 1988). Cooney et al. (1995) demonstrated close

correspondence between the timing of wild juvenile pink salmon ocean entry and the timing

and duration of a coastal springtime zooplankton bloom in Prince William Sound. This

correspondence suggested that fry benefit by emerging during this period. In fact, marine

survival estimates from the hatchery program demonstrate that fry released into the bloom

perform better than fry released prior to, or after, the peak of zooplankton biomass. Until

recently, this observation seemed to confirm food-limited growth dependence for fry, since

juvenile pink salmon are immediate consumers of pelagic food in the deep, nearshore waters

of the region (Urquhart 1979). However, more recent studies (Willette in press) demonstrate

pink salmon fry growth rates (determined from post-release recaptures of wire-tagged fry) are

predicted by springtime temperatures, but not by levels of food. This surprising result means

that either zooplankton is rarely growth-rate limiting for fry, or that plankton plays some yetto-be-determined role in modifying hatchery and, presumably, wild stock production.

In 1993, after a week-long blockade of the Alyeska Pipeline Terminal in Port Valdez

by fishermen concerned over failing pink salmon and herring production following the Exxon

Valdez oil spill, out-of-court settlement funds were made available to pursue ecosystem-level

studies of the early life stages of these two commercial species. In April 1994, the Sound

Ecosystem Assessment (SEA) program began the first of five intensive years of field and

modeling studies. The SEA program attempts a combined bottom-up and top-down approach

to describe factors constraining juvenile pink salmon (and herring) survival. The research

focus is on oceanographically modified predation loss as the principal factor regulating pink

salmon survival in the juvenile stages each year. Mechanisms influencing fry survival are

being used to create a series of physical and biological models envisioned as the major

research products of the work, and as carry-forward tools for more informed management of

Prince William Sound’s pink salmon populations.

In developing its program, SEA began with a simple carbon budget for the region.

Given previous estimates of primary productivity, and adopting accepted transfer
187

efficiencies, carbon fixed by phytoplankton was distributed to zooplankton and higher

consumers. Enough was understood about the growth of juvenile salmon so their forage

demand could be computed on the basis of observed growth rates (Cooney 1993). This

surprisingly small demand was then increased by a factor of 10 to estimate the consumption

for all 0-age fish in the system, including Pacific herring (Clupea pallasi), northern

smoothtongue (Leuroglossus schmidti), and walleye pollock (Theragra chalcogramma). The

remaining carbon was distributed to older juvenile fishes and apex consumers, including

adult fish, birds, and marine mammals (Fig. 3).

The carbon budget suggests that zooplankton should support large populations of

consumers, and that the region may also serve as a juvenile fish nursery. The model further

suggests that when zooplankton stocks are low—seasonally or annually—intermediate and

large-size consumers can augment their diets by eating more smaller fishes. Since the

subarctic surface zooplankton community is greatly diminished during the fall and winter

months, the pelagic system is probably more planktivorous during the spring and summer

months, and piscivorous during much of the remainder of the year. The present research

program focuses on the role that zooplankton and other factors play in modifying losses of

juvenile salmon to predators during the critical first few weeks of early marine residence.

Field studies take advantage of large fry releases from hatcheries to observe and measure

local predation losses on timescales of days to weeks during a sampling period from April

through mid-June.

After 2 years of study, the SEA program has begun to assemble an understanding of

processes regulating the survival of wild and hatchery released juvenile pink salmon. Fry

predator studies have demonstrated that birds (principally kittiwakes) and walleye pollock

play a major role in fry losses each year. Personnel of local hatcheries have been aware of

bird and pollock predation, but they have never attempted a quantitative assessment of the

annual impact. Midwater trawling and acoustic surveys conducted near hatcheries in western

Prince William Sound during the spring and summer of 1994 and 1995 established that adult

pollock from a successful 1988 year class were the most dominant members of the

nearsurface large-fish community from late April through early July. In April and May, a

significant percentage of the diet of these fish was zooplankton; calanoid copepods were

dominant and represented mostly by Neocalanus spp. During both 1994 and 1995, large

numbers of calanoids occurred concurrently in the water column and stomachs of the walleye

pollock. In both years, the consumption of 0-age fishes, including juvenile salmon, declined

or remained at low levels in pollock diets during the copepod bloom (Fig. 4). Since wild and

hatchery stocks of juvenile salmon migrate across deep water each year as they move

southward in the region, offshore losses to adult pollock are probably modified by amounts

of zooplankton present at this time.

In addition to salmon fry being vulnerable to adult walleye pollock over the deeper

passages, more recent results suggest that in late May and early June of some years, 1- and 2-

year-old pollock move into nearshore tidally mixed zones to feed. This is a time when most

fry have grown to 50-70 mm in size and are leaving the shallow waters. Stomach analyses
188

Figure 3. A generalized annual carbon budget for the pelagic ecosystem of Prince William

Sound, Alaska.
189

Figure 4. Adult walleye pollock stomach contents illustrating a time-series of large calanoid

copepods, age-0 fish, and juvenile salmon. The releases of pink salmon from a

nearby hatchery are also shown. The upper set is 1994, the lower, 1995.
190

indicate that some juvenile pollock feed heavily on salmon fry. Depending on the time

phasing and numbers of each year, these late-arriving predators could account for substantial

losses of juvenile pink salmon, particularly during years when reduced fry growth may

extend their nearshore nursery period. The significance of fry size in relation to predation

was examined in 1994 by experimentally releasing some fry that had been grown to over 1-g

live weight. These fish, approximately four times larger than fry normally released from

hatcheries, exhibited marine survivals an order of magnitude higher than their smaller

surviving siblings (Table 1).

Other predators, including adult herring, squid, greenling (Hexagrammos spp.), Dolly

Varden trout (Salvelinus malma), and adult salmon, also prey on juvenile salmon. With the

possible exception of squid, these other predators seem to play a lesser predation role than

walleye pollock. Unfortunately, there are problems associated with quantitatively sampling

most of these other species. Squid are probably not taken adequately in trawls or fixed gear,

and the nearshore regime cannot be fished with trawls because of the steep and rocky local

topography. Seines, gill nets, and traps are providing some qualitative data, and side-scan

sonar may help in the future.

Surprisingly, the monthly tidal cycle is also implicated in the survival of juvenile

salmon. Survival is better under spring-tide rather than neap-tide conditions (Fig. 5).

Observations this past year also demonstrate that catches of adult pollock were statistically

correlated with tidal state. At the height of a mid-May spring-tide series, adults left the upper

layers only to reappear later as the spring cycle relaxed (Fig. 6). We surmise that increased

currents and turbulence associated with larger tidal lenses cause fish populations to reorient

their distributions, and that feeding may be curtailed during these times.

In summary, a combined oceanographic and fisheries study in Prince William Sound

is beginning to describe factors that interact to modify predation losses in juvenile salmon

populations each year. Generally, pink salmon seem to have evolved a life history strategy

that brings the juveniles into marine waters during an intense period of plankton growth each

spring. This timing—on average—provides forage and seasonally warming temperatures that

probably stimulate critical early season growth rates. The presence of immense upper-layer

calanoid populations also provides food for most other consumers during this same time.

Many fish and birds that eat fry find energy in abundant plankton populations as well. For

any given year, the time-space phasing of fry, plankton, and consumer fish and bird

populations, together with ocean temperatures, probably establish the conditions that modify

predation on juvenile pink salmon. Warm years with high zooplankton stocks should enhance

survival of rapidly growing fry that escape predation because most of the energy flowing to

larger fishes, birds, and mammals comes from plankton. In contrast, cold years with reduced

plankton biomass should be disastrous to fry whose growth rates would be reduced and who

would be preyed upon more heavily by larger consumers unable to obtain sufficient energy

from plankton. These extreme examples occur in the historical salmon record. However,

there are enough years when fry growth rate and plankton sheltering alone fail to predict

production to negate the applications of just this information.
191

Table 1. Marine survivals for hatchery pink salmon by release size and date for two

hatcheries in Prince William Sound, 1994.
192

Figure 5. Percent marine survival for fry released at different stages of the monthly tidal

cycle during April and May 1994 and returning as adults in 1995.
193

Figure 6. A time-series of catch, and the relationship between tidal range and catch, of adult

walleye pollock in April, May, and June 1995.
194

Because of inherent system complexities, it is unlikely that our overall results will

ever lend themselves to highly accurate survival estimates of pink salmon based on fry year

growth conditions and predation loss factors. However, we do expect that simulations of

major parts of the system will provide reasonably consistent projections of good, average, or

poor marine survivals one year in advance of adult returns. This consistency is presently

lacking in forecasts of pink salmon in Prince William Sound, to the detriment of local

harvest-management and enhancement programs.

To accomplish this goal, the SEA program is proposing a nominally funded long-term

monitoring program to reinitialize the model(s) for selected bottom-up forcing (temperature,

winds, fresh water, other), for validation purposes, and to index, rather than predict, predator

populations each year. The SEA program is expected to complete by 1997 much of the

modeling and to have a working, constantly updated, forecasting model running by 1999.

Citations

Bax, N. J. 1983. Early marine mortality of marked juvenile chum salmon (Oncorhynchus

keta) released into Hood Canal, Puget Sound, Washington, in 1980. Can. J. Fish.

Aquat. Sci. 40:426-435.

Cooney, R. T. 1993. A theoretical evaluation of the carrying capacity of Prince William

Sound, Alaska, for juvenile Pacific salmon. Fish. Res. 18:77-87.

Cooney, R. T., T. M. Willette, S. Sharr, D. Sharp, and J. Olsen. 1995. The effect of climate

on North Pacific pink salmon (Oncorhynchus gorbuscha) production: Examining

some details of a natural experiment. In R. J. Beamish (editor), Climate change and

northern fish populations. Can. Spec. Publ. Fish. Aquat. Sci. 121:475-482.

Hare, S. R., and R. C. Francis. 1995. Climate change and salmon production in the Northeast

Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations. Can. Spec. Publ. Fish. Aquat. Sci. 121:357-372.

Hargreaves, N. B., and R. J. LeBrassuer. 1985. Species selective predation on juvenile pink

salmon (Oncorhynchus gorbuscha) and chum salmon (O. keta) by coho salmon (O.

kisutch). Can. J. Fish. Aquat. Sci. 42:659-668.

Hartt, A. C. 1980. Juvenile salmon in the oceanic ecosystem—the critical first summer. In W.

J. McNeil and D. C. Himsworth (editors), Salmonid ecosystems of the North Pacific.

Oregon State University Press, Corvallis, p. 25-57.

Healey, M. C. 1982. Timing and relative intensity of size-selective mortality of juvenile

chum salmon (Oncorhynchus keta) during early sea life. Can. J. Fish. Aquat. Sci.

39:952-957.
195

Healey, M. C. 1991. Diets and feeding rates of juvenile pink, chum and sockeye salmon in

Hecate Strait, British Columbia. Trans. Am. Fish. Soc. 120:303-318.

Mortensen, D. G. 1983. Laboratory studies on factors influencing the first feeding of newly

emerged pink salmon (Oncorhynchus gorbuscha) fry. M.S. Thesis, 108 p. Univ.

Alaska, Juneau.

Parker, R. R. 1971. Size selective predation among juvenile salmonid fishes in a British

Columbia inlet. J. Fish. Res. Board Can. 28:1503-1510.

Rogers, D. E. 1986. Pacific salmon. In D. W. Hood and S. T. Zimmerman (editors), The Gulf

of Alaska: Physical environment and biological resources. U.S. Dep. Comm., NOAA,

Environ. Res. Lab., p. 461-478. (Available from Arctic Environ. Assess. Cent., 222

W. 8th Ave., No. 56, Anchorage, AK 99513.)

Taylor, S. G. 1988. Inter- and intra-annual survival of pink salmon (Oncorhynchus

gorbuscha) returning to Auke Creek, Alaska in 1986 and 1987. APPRISE Annual

Report 1987. School of Fisheries and Ocean Sciences, Univ. Alaska, Fairbanks, Tech.

Rep. 1:547-571.

Urquhart, D. L. 1979. The feeding, movement, and growth of pink salmon (Oncorhynchus

gorbuscha) fry released from a hatchery in Prince William Sound, Alaska. M.S.

Thesis, Univ. Alaska, Fairbanks, 111 p.

Walters, C. J., J. Holborn, R. M. Peterman, and M. J. Staley. 1978. Model for examining

early ocean limitation on Pacific salmon production. J. Fish. Res. Board Can.

35:1303-1315.

Willette, T. M. 1985. The effects of ocean temperatures on the survival of odd- and even-year

pink salmon (Oncorhynchus gorbuscha) populations originating from Prince William

Sound, Alaska. M.S. Thesis, Univ. Alaska, Fairbanks, 115 p.

Willette, T. M. In press. Impacts of the Exxon Valdez oil spill on the migration, growth and

survival of juvenile pink salmon in Prince William Sound, Alaska. Proceedings of

EVOS Symposium, Feb. 1993, Anchorage, Alaska.

Willette, T. M., and R. T. Cooney. 1991. An empirical orthogonal functions analysis of sea

surface temperature anomalies in the North Pacific Ocean and cross correlations with

pink salmon (Oncorhynchus gorbuscha) returns to southern Alaska. In B. White and

I. Guthrie (editors), Proceedings of 15th Pink and Chum Salmon Workshop. Pacific

Salmon Commission, p. 111-121. (Available from Pacific Salmon Commission, 600-

1155 Robson St., Vancouver, BC, Canada V6E 1B9.)
196
197

THE IMPORTANCE OF VARIOUS SPATIAL AND TEMPORAL SCALES IN THE

INTERACTION OF JUVENILE SALMON AND THE MARINE ENVIRONMENT

Richard D. Brodeur

Alaska Fisheries Science Center

National Marine Fisheries Service

7600 Sand Point Way NE

Seattle, WA 98115-0070

Physical and biological oceanographers have long recognized the various scales of

spatial and temporal variability affecting ecological processes in the ocean (Denman and

Powell 1984, Legendre and Demers 1984, Haury and Pieper 1987, Steele 1978, Mann and

Lazier 1991, Dickey 1990). The purpose of this paper is to examine several of the spatial and

temporal scales of variability that Pacific salmon (Oncorhynchus spp.) are exposed to during

their early life in the ocean, and discuss how these may specifically affect the feeding

ecology of these juveniles. The scales of variability encountered by an individual salmon

may be broad in terms of spatial extent, from those affecting the few meters immediately

nearby to those affecting much of the Pacific basin. Similarly, processes that occur on

temporal scales ranging from a few minutes to several decades may be important. Some of

the spatial and temporal scales of variability that may be important to the feeding of juvenile

salmon are shown in Figure 1.

It is beyond the scope of this paper to examine in detail all of these physical factors. I

will instead focus on three of these which may be particularly important. Included among

these are long-term interannual cycles of variability which may be affected, such as that seen

for El Niño events, by physical forcing mechanisms initiated well beyond the waters of the

Pacific Northwest. I will also look at a mesoscale feature, such as the dynamics of the

Columbia River plume, which may be important for only a few months and in only part of

the oceanic range of a salmon species. Finally, I will examine small-scale features, such as

Langmuir circulation cells and internal waves, and suggest how these may also be important

to the feeding ecology of juvenile salmon.

Large-Scale Variability

Long time series, extending, for example, back to the early part of the century, are

now available for several environmental and biological variables in the North Pacific (e.g.,

Beamish 1995). Several areas, notably the California Cooperative Oceanic Fisheries

Investigations grid and Ocean Station P, have been intensely studied for several decades and

provide some measure of the interannual variability occurring on a local scale (Brodeur et al.

1996). Superimposed upon this shorter term interannual variability is the longer scale

environmental variability associated, for instance, with the El Niño/Southern Oscillation
198

Figure 1. Time and space scales of physical variability in the ocean environment which may

affect juvenile salmon.
199

(ENSO) phenomenon. Although ENSO warming events are known to occur on the order of

every 3-4 years, it is only every 25 years on average when an event is of sufficient strength to

affect high latitude ecosystems. An event occurring during 1982-83 was one of the strongest

and best documented on record (Mysak 1986, Pearcy and Schoener 1987) and had substantial

negative impacts on adult salmon production (Pearcy et al. 1985, Mysak 1986, Johnson

1988). I will present some possible ways in which an ENSO event may affect juvenile

salmon feeding and subsequent survival.

One of the most direct ways in which an El Niño may affect salmon may be in the

suppression of normal upwelling conditions in coastal waters. Several studies have shown a

strong relationship between the survival and growth of coho salmon (Oncorhynchus kisutch)

and the upwelling intensity when they first entered the ocean (Scarnecchia 1981, Nickelson

1986, Fisher and Pearcy 1988). For example, mean monthly Bakun upwelling indices were

far below normal during the summer of 1983, resulting in high surface temperatures and low

chlorophyll a concentrations along much of the West Coast (Fiedler 1984, Brodeur and

Pearcy 1992). Even when upwelling conditions were favorable, a strong and deep

thermocline, caused by onshore and northward advection of warm water, prevented normal

mixing and resulted in warm, nutrient- poor water being upwelled to the surface (Huyer and

Smith 1985).

The reduced upwelling may have greatly affected the entire pelagic ecosystem off

Oregon and Washington, resulting in less overall food and a shift in the diets of most pelagic

predators, including juvenile and adult salmon, to less preferred prey items (Brodeur and

Pearcy 1990, 1992). Although the mean stomach fullness of juvenile salmon was not

significantly different than in other non-Niño years (Brodeur 1992), the prey composition

was radically different, consisting of smaller and probably less nutritious zooplankton species

instead of the euphausiids and larval and juvenile fishes normally consumed by juvenile

salmon (Pearcy et al. 1985, Brodeur and Pearcy 1990). As Fulton and LeBrasseur (1985)

have shown, a major northward shift in the Subarctic Boundary occurs during strong ENSO

events (Fig. 2), which results in a smaller prey-size spectrum of available food organisms,

which may not be used as efficiently by juvenile salmon.

Other ways in which an ENSO warming event may influence survival of salmon is by

changing their migration and distribution patterns, making them more available or

susceptible to predators (Mysak 1986). The intrusion of warm oligotrophic waters onto the

shelf may limit the distribution of salmon to a much narrower nearshore zone. If the offshore

abundance of alternate prey species is also reduced during an El Niño year, the

concentrations of juveniles may attract avian and piscine predators (Pearcy 1988). A decrease

in mean growth rate expected under low productivity would potentially increase the

probability of salmon being consumed by a size-selective predator (Healey 1982).

Furthermore, if concentrations of prey resources are much lower, the salmon must

expend a much greater amount of time searching for food at a greater energy expenditure

while being able to spend less time avoiding predators. The higher temperatures also

necessitate higher rations to sustain the increased metabolic rates. Juvenile coho and chinook
200

Figure 2. Interannual shifting of the Subarctic Boundary during warm and cold years (from

Fulton and LeBrasseur 1985).
201

salmon (O. tshawytscha) food consumption during 1983, based on bioenergetic modeling

estimates, indicated that both species were food limited due to the higher rations and

decreased food availability during ENSO conditions (Brodeur et al. 1992). During normal

years, there appeared to be adequate food for juvenile salmon survival.

Mesoscale Variability

An example of a mesoscale feature affecting mainly Oregon and Washington coastal

waters and lasting several months is the dynamic nature of the Columbia River plume. At the

height of its development, this oceanic extension of the Columbia River extends well

offshore and south to off central Oregon. According to Barnes et al. (1972), its outer

boundary is delimited by the 32.5‰ isohaline. During the winter, the outflow from the

Columbia River is much weaker and the winds are from the southwest which pushes the

plume onto the Washington coast. During a period called the spring transition in April-May,

the prevailing wind pattern switches to northerly winds and the plume moves south. The

winds also promote inshore coastal upwelling which pushes the plume well offshore (Fig. 3),

although the shape and orientation of the plume can be variable during the summer (Fiedler

and Laurs 1990). During the period of maximum runoff, the equivalent height of fresh water

averages about 1 m (Barnes et al. 1972).

There is some evidence that juvenile coho salmon originating from the Columbia

River utilize the plume as a transitional “habitat” between the brackish estuary and high

salinity oceanic water. Marked juveniles caught at sea appear to follow the plume southward,

travelling at about the same speed as the alongshore currents (Pearcy and Fisher 1988). It is

only late in the summer or during poor upwelling years when the plume breaks down that

juvenile coho begin to move northward. The timing of events also appears to be important.

There appears to be a strong relationship between the date of the spring transition and the

subsequent survival of the year class of coho salmon (Zirges 1981). Presumably, fish which

enter the ocean before or shortly after the transition encounter a turbulent and highly saline

environment, whereas later migrants that enter into a well-developed plume would enter a

relatively benign environment and could gradually adjust to oceanic conditions. Riverine

plumes also tend to have higher concentrations of zooplankton prey relative to adjacent

marine waters, especially along the plume frontal region, which may attract juvenile salmon

(St. John et al. 1992).

The date of transition can be variable on an interannual basis, extending from late

January to May. The approximate timing of this transition can be deduced by examining for

abrupt changes in the daily Bakun upwelling index or sea level, although in some years the

transition is not well demarcated using these methods. A direct although costly method

would be to examine moored surface current-meter data. An alternate method might be to use

satellite temperature and ocean color imagery which can delineate the plume from adjacent

upwelling and oceanic water (Pearcy and Keene 1974, Fiedler and Laurs 1990). The use of

satellites may be an important tool for future salmon fisheries managers (Fiedler et al. 1984).
202

Figure 3. Seasonal variation in the location of the Columbia River plume (from Barnes et al.

1972). The plume is delimited by a dashed line in the figures.
203

In addition to the initial effects that the timing of the transition date has on the

survival of salmon, the date of the transition between winter and summer regimes appears to

be inversely related to the total cumulative upwelling occurring during any particular summer

(Fig. 4). Although the long-term mean discharge of the Columbia River appears to be

relatively constant, there has been a decrease over the last several decades in the volume of

water exiting the Columbia River during peak outflow periods (Fig. 5) which may affect the

thickness and offshore extent of the plume. The Fraser River system, which has less

hydroelectric development and agricultural diversions than the Columbia River system, does

not show a similar decrease in peak flow (Fig. 5). It is uncertain whether climatic-scale

changes in precipitation patterns or anthropogenic changes (water storage and irrigation) is

the main cause of this decrease, but it may possibly have serious consequences for salmon

production in the Columbia River.

Small-Scale Variability

Small-scale variability refers to processes that may last only hours or even minutes

and may affect the immediate surroundings of an individual juvenile salmon. Two such

processes affecting surface waters are wind-driven vortical circulation such as Langmuir cells

(Barstow 1983) and wave packets formed by internal waves (Owen 1981). Both of these

processes form long rows of aggregated materials evident as slicks on the surface; the main

difference being that the Langmuir cells are oriented in the direction of the wind while the

internal waves do not necessarily have to be (Fig. 6). Because of their circulation patterns,

both these processes have been shown to concentrate zooplankton in the neuston layer at

densities several orders of magnitude above the surrounding surface and subsurface waters

(Shanks and Wright 1987, Shenker 1988), which may in turn attract juvenile fish which feed

on these concentrations (Kingsford and Choat 1986).

I have hypothesized (Brodeur 1989) that foraging juvenile salmon may utilize these

food concentrations to some degree to minimize the search area needed to satisfy their daily

energy requirements. The species composition found in neuston net tows bears a distinct

similarity to those found in the stomachs of juvenile coho salmon. Some major food items,

such as crab megalopae, are found in such high abundances in these aggregations that they

may be visible from the deck of a ship (Shenker 1988). There is evidence that coho salmon

reside in the upper 2 m of the water column at night (Pearcy and Fisher 1988) and may take

advantage of these prey patches while minimizing predation upon themselves by visual

surface predators such as seabirds. The dynamics of small-scale wind and wave motions may

thus be linked to the feeding and hence survival of these juveniles.

Other Processes

Physical processes that occur on many different scales of variability appear to be

important to the ecology of juvenile coho salmon. In addition to the three factors that are
204

Figure 4. Relationship between relative transition date (May 1 = 0) and cumulative daily

upwelling strength (cubic meters per second per 100 m of coastline) from March

through September at 42°N 125°W. Upwelling data through 1981 are from

Nickelson (1986), and the remaining years were calculated from data in Mason and

Bakun (1986). The regression equation is fit to all years with the exception of

1983 (-28, 177) which was considered an anomalous year.
205

Figure 5. Comparison of monthly means (heavy lines) and the minimum and maximum

monthly values (thin lines) for the Columbia River and the Fraser river (from

Francis et al. (1989) and P. LeBlond, University of British Columbia, unpubl.

data).
206

Figure 6. Convergence zones in surface waters created by Langmuir circulation (upper) and

internal waves (lower). Upper figure is from Barstow (1983) and lower figure is

from Shanks and Wright (1987).
207

discussed here, other processes such as long-term environmental trends and regime shifts

(McLain 1984, Francis and Hare 1994, Brodeur et al. 1996), upwelling intensity (Nickelson

1986), and coastal currents (Pearcy and Fisher 1988) may also be important. Upwelling

intensity appears to be the most important factor controlling food production in the coastal

zone for juvenile salmon. Both the duration of upwelling events as well as the absolute

intensity over the entire upwelling season may be important (Cury and Roy 1989). Excessive

or persistent upwelling-favorable winds may be detrimental to coastal primary production in

that nutrient-rich waters will be continuously advected offshore (Small and Menzies 1981).

Clearly, comprehensive reviews of oceanographic factors affecting juvenile salmon,

such as those by Tabata (1984) for sockeye salmon (O. nerka) off British Columbia and

Pearcy (1992) for coho salmon off Oregon and Washington, should be desirable reading for

any biologist intending to do research on ocean salmon survival. We can no longer afford to

ignore the variability inherent in the marine system when studying the variability in ocean

survival. Salmon biologists would be wise to interact with physical oceanographers or at least

become cognizant of many physical processes likely to affect the ecology of salmon in the

ocean.

Citations

Barnes, C. A., A. C. Duxbury, and B. A. Morse. 1972. Circulation and selected properties of

the Columbia River effluent at sea. In A. T. Pruter and D. L. Alverson (editors), The

Columbia River estuary and adjacent ocean waters, p. 41-80. Univ. Washington

Press, Seattle.

Barstow, S. F. 1983. The ecology of Langmuir circulation: A review. Mar. Environ. Res.

9:211-236.

Beamish, R. J. (editor). 1995. Climate change and northern fish populations. Can. Spec. Pub.

Fish. Aquat. Sci. 121:1-739.

Brodeur, R. D. 1989. Neustonic feeding by juvenile salmonids in coastal waters of the

Northeast Pacific. Can. J. Zool. 67:1995-2007.

Brodeur, R. D. 1992. Factors related to variability in feeding intensity of juvenile coho and

chinook salmon. Trans. Am. Fish. Soc. 121:104-114.

Brodeur, R. D., R. C. Francis, and W. G. Pearcy. 1992. Food consumption of juvenile coho

(Oncorhynchus kisutch) and chinook salmon (O. tshawytscha) on the continental

shelf off Washington and Oregon. Can. J. Fish. Aquat. Sci. 49:1670-1685.
208

Brodeur, R. D., B. W. Frost, S. R. Hare, R. C. Francis, and W. J. Ingraham, Jr. 1996.

Interannual variations in zooplankton biomass in the Gulf of Alaska and covariation

with California Current zooplankton biomass. Calif. Coop. Oceanic Fish. Invest. Rep.

37:80-99.

Brodeur, R. D., and W. G. Pearcy. 1990. Trophic relations of juvenile Pacific salmon off the

Oregon and Washington coast. Fish. Bull., U.S. 88:617-636.

Brodeur, R. D., and W. G. Pearcy. 1992. Effects of environmental variability on trophic

interactions and food web structure in a pelagic upwelling ecosystem. Mar. Ecol.

Prog. Ser. 84:101-118.

Cury, P., and C. Roy. 1989. Optimal environmental window and pelagic fish recruitment

success in upwelling areas. Can. J. Fish. Aquat. Sci. 46:670-680.

Denman, K. L., and T. M. Powell. 1984. Effects of physical processes on planktonic

ecosystems in the coastal ocean. Ocean. Mar. Biol. Ann. Rev. 22:125-168.

Dickey, T. D. 1990. Physical-optical-biological scales relevant to recruitment in large marine

ecosystems. In K. Sherman, L. M. Alexander, and B. D. Gold (editors), Large marine

ecosystems: Patterns, processes, and yields, p. 82-98. Am. Assoc. Adv. Sci. Publ. 90-

305.

Fiedler, P. C. 1984. Satellite observations of the 1982-1983 El Niño along the U.S. Pacific

Coast. Science 224:1251-1254.

Fiedler, P. C., and R. M. Laurs. 1990. Variability of the Columbia River plume observed in

visible and infrared satellite imagery. Int. J. Remote Sens. 11:999-1010.

Fiedler, P. C., G. B. Smith, and R. M. Laurs. 1984. Fisheries applications of satellite data in

the eastern North Pacific. Mar. Fish. Rev. 46:1-13.

Fisher, J. P., and W. G. Pearcy. 1988. Growth of juvenile coho salmon (Oncorhynchus

kisutch) in the ocean off Oregon and Washington, USA, in years of differing coastal

upwelling. Can. J. Fish. Aquat. Sci. 45:1036-1044.

Francis, R. C., and S. R. Hare. 1994. Decadal-scale regime shifts in the large marine

ecosystems of the North-east Pacific: A case for historical science. Fish. Oceanogr.

3:279-291.

Francis, R. C., W. G. Pearcy, R. D. Brodeur, J. P. Fisher, and L. Stevens. 1989. Effects of the

ocean environment on the survival of juvenile salmonids. Univ. Washington, Fish.

Res. Inst. Rep., Seattle, 34 p.
209

Fulton, J. D., and R. J. LeBrasseur. 1985. Interannual shifting of the subarctic boundary and

some of the biotic effects on juvenile salmonids. In W. S. Wooster and D. L. Fluharty

(editors), El Niño North: Niño effects in the eastern subarctic Pacific, p. 237-247.

Washington Sea Grant Program, Univ. Washington, Seattle. Publ. WSG-WO-85-3.

Haury, L. R., and R. E. Pieper. 1987. Zooplankton: scales of biological and physical events.

In D. F. Soule and G. S. Kleppel (editors), Marine organisms as indicators, p. 35-72.

Springer Verlag, New York.

Healey, M. C. 1982. Timing and relative intensity of size-selected mortality of juvenile chum

salmon (Oncorhynchus keta) during early sea life. Can. J. Fish. Aquat. Sci. 39:952-

957.

Huyer, A., and R. L Smith. 1985. The signature of El Niño off Oregon, 1982-1983. J.

Geophys. Res. 90:7133-7142.

Johnson, S. L. 1988. The effects of the 1983 El Niño on Oregon’s coho (Oncorhynchus

kisutch) and chinook (O. tshawytscha) salmon. Fish. Res. 6:105-123.

Kingsford, M. J., and J. H. Choat. 1986. Influence of surface slicks on the distribution and

onshore movements of small fish. Mar. Biol. 91:161-171.

Legendre, L., and S. Demers. 1984. Towards dynamic biological oceanography and

limnology. Can. J. Fish. Aquat. Sci. 41:2-19.

Mann, K. H., and J. R. N. Lazier. 1991. Dynamics of marine ecosytems. Blackwell Scientific

Publications, Cambridge, MA, 467 p.

Mason, J. E., and A. Bakun. 1986. Upwelling index update, U.S. West Coast, 33°N-48°N

latitude. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-SWFC 67; 81 p.

McLain, D. R. 1984. Coastal ocean warming in the Northeast Pacific, 1976-83. In W. G.

Pearcy (editor), The influence of ocean conditions on the production of salmonids in

the North Pacific, p. 61-86. Oregon Sea Grant Program, Oregon State Univ.,

Corvallis. Publ. ORESU-W-83-001.

Mysak, L. A. 1986. El Niño, interannual variability and fisheries in the Northeast Pacific

Ocean. Can. J. Fish. Aquat. Sci. 43:464-497.

Nickelson, T. E. 1986. Influences of upwelling, ocean temperature, and smolt abundance on

marine survival of coho salmon (Oncorhynchus kisutch) in the Oregon production

area. Can. J. Fish. Aquat. Sci. 43:527-535.
210

Owen, R. W. 1981. Fronts and eddies in the sea: mechanisms, interactions and biological

effects. In A. R. Longhurst (editor), Analysis of marine ecosystems, p. 197-233.

Academic Press, New York.

Pearcy, W. G. 1988. Factors affecting survival of coho salmon off Oregon and Washington.

In W. J. McNeil (editor), Salmon production, management, and allocation, p. 67-73.

Oregon State Univ. Press, Corvallis.

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Univ. Washington Press,

Seattle, 179 p.

Pearcy, W. G., and J. P. Fisher. 1988. Migrations of coho salmon, Oncorhynchus kisutch,

during their first summer in the ocean. Fish. Bull., U.S. 86:173-195.

Pearcy, W., J. Fisher, R. Brodeur, and S. Johnson. 1985. Effects of the 1983 El Niño on

coastal nekton off Oregon and Washington. In W. S. Wooster and D. L. Fluharty

(editor), El Niño North: Niño effects in the eastern subarctic Pacific, p. 188-204.

Washington Sea Grant Program, Univ. Washington, Seattle. Publ. WSG-WO-85-3.

Pearcy, W. G., and D. F. Keene. 1974. Remote sensing of water color and sea surface

temperatures off the Oregon coast. Limnol. Ocean. 19:573-583.

Pearcy, W. G., and A. Schoener. 1987. Changes in the marine biota coincident with the 1982-

1983 El Niño in the northeastern subarctic Pacific Ocean. J. Geophysical Res.

92:14417-14428.

Scarnecchia, D. L. 1981. Effects of streamflow and upwelling on yield of wild coho salmon

(Oncorhynchus kisutch) in Oregon. Can. J. Fish. Aquat. Sci. 38:471-475.

Shanks, A. L., and W. G. Wright. 1987. Internal-wave-mediated shoreward transport of

cyprids, megalopae, and gammarids and correlated longshore differences in the

settling rate of intertidal barnacles. J. Exp. Mar. Biol. Ecol. 114:1-13.

Shenker, J. M. 1988. Oceanographic associations of neustonic larval and juvenile fishes and

Dungeness crab megalopae off Oregon, 1984. Fish. Bull., U.S. 86:299-317.

Small, L. F., and D. W. Menzies. 1981. Patterns of primary productivity and biomass in a

coastal upwelling region. Deep-Sea Res. 28:123-149.

Steele, J. (editor). 1978. Spatial pattern in plankton communities. Plenum Press, New York,

470 p.

St. John. M. A., J. S. Macdonald, P. J. Harrison, R. J. Beamish, and E. Choromanski. 1992.

The Fraser River plume: some preliminary observations on the distribution of

juvenile salmon, herring, and their prey. Fish. Ocean. 1:153-162.
211

Tabata, S. 1984. Oceanographic factors influencing the distribution, migration, and survival

of salmonids in the Northeast Pacific Ocean—A review. In W. G. Pearcy (editor),

The influence of ocean conditions on the production of salmonids in the North

Pacific, p. 128-160. Oregon Sea Grant Program, Oregon State Univ., Corvallis. Publ.

ORESU-W-83-001.

Zirges, M. H. 1981. A hypothesis for coho salmon survival mechanisms. Coho Salmon

Management Plan. Oregon Dep. Fish and Wildlife, Newport.
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213

CLIMATE-OCEAN CHANGES AND THE IMPACTS ON

YOUNG SALMON IN THE STRAIT OF GEORGIA

R. J. Beamish and C. Neville

Fisheries and Oceans Canada

Pacific Biological Station

Nanaimo, BC Canada V9R 5K6

The climate event that occurred in the winter of 1976-77 resulted in changes in the

ocean that altered the productivity trends of a number of commercially important fishes. The

effects were particularly noticeable in salmon stocks. The productivity of pink

(Oncorhynchus gorbuscha), chum (O. keta), and sockeye (O. nerka) salmon stocks that

reared in the subarctic Pacific increased, while the productivity of coho (O. kisutch) and

chinook (O. tshawytscha) salmon stocks in the Strait of Georgia and probably off the coasts

of Washington and Oregon decreased. The synchrony of the changes and the use of hatchery

reared smolts to maintain the total production of smolts leaves little doubt that the marine

changes were largely responsible for the declines in productivity of these coastal stocks.

Catches of chinook salmon in the Strait of Georgia began to decline in 1979 (Fig. 1).

Synchronous with this decline was an abrupt and precipitous decrease in marine survival

from an average of 4.8% from 1974 to 1977 (year to sea) to 0.7% from 1978 to 1988 (year to

sea). If overfishing was the major cause of the decline, there would be a gradual reduction in

smolt production at the time of the decrease in catch and marine survival. However, the total

number of wild and hatchery reared chinook salmon smolts produced after the declines

actually increased from a yearly average of about 30 x 106 from 1974-76 to about 82 x 106 in

the early 1990s (Beamish et al. 1995).

There was a decline in coho salmon survival shortly after the decrease occurred for

chinook salmon (Fig. 2). Although the average catch of coho salmon in the Strait of Georgia

remained about the same, there was an increase in smolt production from about 15 x 106

before the change in survival to about 25 x 106 smolts in the early 1990s. Because the marine

mortality for hatchery reared and wild coho salmon is about equal, it is clear that the addition

of smolts to the Strait of Georgia did not increase the total abundance of post-juvenile fish

over the pre-1977 levels.

The changes that occurred in the abundance and survival of chinook and coho salmon

in the Strait of Georgia were coincident with several key physical changes that in turn were

coincident with other major climate-ocean changes that occurred in the winter of 1976-77.

The common factor affecting both of these ecosystems was the Aleutian low pressure system.

The intensification of the low in the late 1970s increased production of salmon species

resident in the offshore areas, possibly through increases in mid-ocean upwelling. The

linkages with the ecosystem in the Strait of Georgia are not well understood, but they
214

Figure 1. Commercial and sport catch of chinook salmon in the Strait of Georgia showing a

declining catch beginning in 1976. The decline in hatchery survival occurred at

about the same time. The releases from Strait of Georgia increased as the catches

declined.
215

Figure 2. Survival of coho salmon from the Strait of Georgia and Fraser River hatcheries.

There was a decline in average survival about 1978, approximately the same time

as for chinook salmon.
216

involved decreases in the snowpack and subsequently in the annual flows of the Fraser River.

At the same time that the trend in flows started to decline, there was an increase in the bottom

and surface temperatures in the strait. The reasons for the increases in temperatures are

unknown as are the relationships with the production of coho and chinook salmon; however,

it is clear that the changes would affect the Strait of Georgia ecosystem. It is also clear that

the message for fisheries management is that it is necessary to understand both the natural

and human factors affecting coho and chinook salmon abundance.

Beginning about 1989, there was another change in the climate-ocean system. In the

tropical Pacific, the change appeared as a persistent and strong negative anomaly of the

Southern Oscillation Index that was associated with higher sea surface temperatures

(Trenberth and Hoar 1996). In the subarctic Pacific, sea surface temperature anomalies

indicated that some warming in the central subarctic Pacific had occurred (Deser et al. 1996)

and there were changes in the trend of the Aleutian low pressure system and other large-scale

climate indices (Beamish et al. in prep.).

In the Strait of Georgia, there was continued warming of the surface and bottom

layers. There also were larger discharges in April from the Fraser River than occurred in the

past (Fig. 3). These larger spring discharges are important because they affect the timing of

the spring plankton bloom. Associated with the change in the pattern of the April flows was a

trend for coho salmon from the Strait of Georgia to move out of the strait (Fig. 4) and rear off

the west coast of Vancouver Island. This is noteworthy because coho salmon fishing in the

Strait of Georgia supports one of the most important recreational fisheries in Canada. For

example, in past years at the same time of this meeting, there would be a rather substantial

fishery for juvenile coho salmon. Our recent studies for this year indicate that there are

virtually no coho salmon in the strait.

We suspect that the ecosystem in the Strait of Georgia changed again when the

physical indices changed about 1989-90. We observed increases in the survival and

abundance of Pacific hake (Merluccius productus) as well as observing that large numbers of

chum salmon remained in the strait longer than they did in the past. There also is an

indication that Pacific herring (Clupea pallasi) are in high abundance. In association with our

colleagues, we are carrying out a 3-year study of the physical and biological factors that

cause these regime shifts.

Regimes are a new and important concept in the management of Pacific salmon. A

productivity regime can be considered to be the level of production within a particular

ecosystem. While it is this level of production that is important for fish stocks, it is the

change in regimes that is an important reference point for managers. It has been assumed in

the past that the survival of salmon in the ocean is either without a long-term trend or that the

highest, historic levels of production represent the upper limits of the possible marine

production. The concept of regime shifts in which the equilibrium level of production

abruptly increases or decreases has, in general, not been considered to be an important part of

Pacific salmon management.
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218
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220

For fish populations, a regime shift is a change in production that is coincident with

climate-ocean changes that result in a response that is synchronous for a number of species

(or stocks), usually over a relatively large area. According to this definition, it is an abrupt

change in equilibrium production that is important and not a reversal in a fluctuating trend.

The changes in both 1976-77 and 1989-90, although different, would be regime shifts

according to our definition. In general, the 1976-77 shift included a temperature reversal and

a change (increase) in the intensity of the Aleutian low. The 1989-90 change appeared as a

change to higher temperatures in some areas as well as a change (decrease) in the intensity of

the Aleutian low pressure system.

It is now 20 years after the 1976-77 event occurred and there is still no explanation of

the cause of the event. There is growing acceptance of the impact on fishes and increasing

evidence linking the climate trends in the tropical Pacific to the changes observed in the

ocean, but there is no explanation of the mechanisms involved. Although the events cannot

be controlled as we attempt to do for fishing effects, the effects of the regime shifts have

profound impacts on regional economies. For example, it is clear when one looks at the

history of the total catches of all Pacific salmon in British Columbia (Fig. 5) that the recent

low catches and resulting economic hardships are in some way associated with climate

effects. There are also associated impacts on the effectiveness of government expenditures

and programs and on the credibility of fisheries studies. The most serious impact, however,

may be in relation to our ability to detect and adapt to the effects on our fisheries caused by a

general warming of our climate.

Citations

Beamish, R. J., G. A. McFarlane, and D. Noakes. In prep. Evidence that decadal scale

changes in global processes are linked to natural shifts in production of Pacific

salmon. (Available from Canadian Department of Fisheries and Oceans, Pacific

Biological Station, Nanaimo, B.C., Canada V9R 5K6.)

Beamish, R. J., B. E. Riddell, C. M. Neville, B. L. Thomson, and Z. Zhang. 1995. Declines in

chinook salmon catches in the Strait of Georgia in relation to shifts in the marine

environment. Fish. Ocean. 4(3):243-256.

Deser, C., M. Alexander, and M. Timlin. 1996. Upper-ocean thermal variations in the North

Pacific during 1970-91. J. Climate 9:1840-1855.

Trenberth, K. E., and T. J. Hoar. 1996. The 1990-1995 El Niño-Southern Oscillation event:

Longest on record. Geophys. Res. Letters. 23(1):57-60.
221

EARLY OCEAN SURVIVAL OF SALMON OFF BRITISH COLUMBIA

AND IMPACTS OF THE 1983 AND 1991-95 EL NIÑO EVENTS

Brent N. Hargreaves

Canadian Department of Fisheries and Oceans

Biological Sciences Branch

Pacific Biological Station

Nanaimo, BC Canada V9R 5K6

Chinook salmon (Oncorhynchus tshawytscha) from the west coast of Vancouver

Island (WCVI) have become a major contributor to commercial troll and recreational

fisheries in British Columbia and southeast Alaska. The Somass River/Robertson Creek

chinook stock is the most important WCVI stock, with total production exceeding 400,000

adults as recently as 1991. However, marine survival rates of this stock have varied by over

two orders of magnitude.

Chinook salmon produced by this stock in a given year can return as 2-, 3-, 4-, 5-, or

6-year-old adults. Although only a small percentage return as 2-year-old males (jacks), once

returns from these younger fish are known, the total return for that brood year for all years

can be reliably forecast. This indicates that marine survival patterns are predominantly

determined during the first year of marine life, before the first jacks return.

Variations in ocean conditions appear to strongly affect marine survival of WCVI

chinook salmon stocks. The lowest marine survival rates observed previously for the Somass

stock (0.1% for the 1983 brood year) coincided with the 1983 El Niño event. This effect was

relatively modest, however, since only one brood year was affected. More recent El Niño

events in 1991-95 have affected survival for at least three consecutive brood years (1990 to

1992), and this has had a much greater impact. The returns of WCVI chinook salmon in 1995

were low, and returns in 1996 and 1997 are forecast to be extremely poor. Predation on

juvenile chinook salmon during the early marine period was likely a major cause of the poor

survivals of the 1983 and 1991-93 brood years. The cause of the longer term pattern of

declining survival rates which preceded both of these major El Niño events is not known.
222
223

Process and Mechanisms—Offshore Marine
224
225

OFFSHORE DISTRIBUTION AND MIGRATION PATTERNS

AND OCEAN SURVIVAL OF SALMON

Katherine W. Myers

Fisheries Research Institute

University of Washington

Box 357980, Seattle, WA 98195-7980

Almost all data (1955-92) on offshore distribution and migration patterns of

northeastern Pacific salmon (Oncorhynchus spp.) were obtained by the national research

programs of the member nations of the former International North Pacific Fisheries

Commission (INPFC). The results of much of the research through the early 1970s are

summarized by species in five joint-comprehensive reports issued by INPFC on coho (O.

kisutch; Godfrey et al. 1975), sockeye (O. nerka; French et al. 1976), chum (O. keta; Neave

et al. 1976), chinook (O. tshawytscha; Major et al. 1978), and pink (O. gorbuscha; Takagi et

al. 1981) salmon. More recently, reports were issued on offshore distribution and migration

patterns of steelhead (O. mykiss; Burgner et al. 1992), and on the distribution and origins of

salmon and steelhead in the area of the former Japanese land-based driftnet salmon fishery,

south of lat. 46°N (Myers et al. 1993). The final Bulletin in the INPFC series included

information on distribution of salmon and steelhead in the area of the former squid driftnet

fisheries (e.g., Pella et al. 1993).

The primary objective of the historical U.S. and Canadian offshore research was to

determine if the Japanese high seas driftnet fisheries were catching North American salmon.

Before 1978, field research was concentrated in the times (primarily May-July) and areas of

the Japanese mothership salmon driftnet fisheries, particularly in the vicinity of the INPFC

abstention line along meridian 175°W, which was the eastern boundary of Japanese salmon

fishing. With the implementation of U.S.S.R. and U.S. 200-mile zones in 1977-78, the times,

areas, and fishing quotas of the Japanese fisheries were reduced. In 1978, the eastern

boundary of the fishery was moved to long. 175°E, and research emphasis shifted to

identifying the continent of origin of salmonids caught by the expanding Japanese land-based

driftnet fishery in the offshore area south of 46°N. In the late 1980s and early 1990s, as the

times, areas, and catch quotas of the salmon driftnet fisheries were further reduced, research

emphasis shifted again to determining the bycatch of salmonids by the rapidly developing

Asian squid driftnet fisheries in the area south of 46°N and west of 140°W.

The historical data are not adequate to provide a good understanding of the offshore

distribution and migration patterns of northeastern Pacific salmonids. Most of the research in

the Gulf of Alaska, which is the major offshore rearing area for many northeastern Pacific

salmon populations, was done opportunistically during the 1950s and 1960s, primarily in

spring and summer (April-August). Data from offshore areas south of the Gulf of Alaska

(south of 50°N) and off the U.S. West Coast are particularly limited. Spatial and temporal
226

distribution of sampling effort and the types of gear used to catch salmon varied. Almost all

salmon catches were by surface gear (gillnet, longlines, and purse seines), and they do not

provide information on vertical distribution of salmon. Sea surface temperature was often the

only oceanographic data collected. There have been significant changes in abundance and

composition of northeastern Pacific salmon populations since the mid-1960s (e.g., Rogers

1986). In addition, there have been major changes in North Pacific climate and oceanography

since the mid-1960s (summarized by Trenberth and Hurrell 1995).

The historical data have been used to develop conceptual models of seasonal offshore

distribution and migration patterns of northeastern Pacific salmon by combining observations

from all gear types and years (e.g., Neave et al. 1976, French et al. 1976, Takagi et al. 1981).

The models do not provide information on discrete populations or on interannual variation in

distribution and migration patterns, and they need to be validated with new field data.

High seas tag recovery data (1955-95) provide limited evidence that offshore

distribution and migration patterns of Pacific salmon are population-specific. The most

extensive data are for sockeye salmon, which were the major focus of the historical U.S. and

Canadian research programs. These data clearly show that Asian and North American

sockeye have different ocean ranges (Fig. 1A). North American populations from large lake

or river systems also have broadly overlapping but different ocean ranges (e.g., Bristol Bay

and Fraser River, Fig. 1A). Analyses of the tag data with respect to expected returns

indicated that Bristol Bay fish with different early life histories have different ocean

distribution and migration patterns (Rogers 1986; Fig. 1B). The high seas tag data are not

adequate to determine offshore distributions of discrete populations of northeastern Pacific

salmon because the majority of recoveries were made in coastal, mixed-stock fisheries.

Many scientists have concluded from the historical data that offshore movements of

Pacific salmon are not random and involve sophisticated orientation or true navigation

(e.g., Quinn 1991). Tagging and tracking studies show that movements of individual adult

Pacific salmon returning from offshore to coastal waters are rapid and direct (e.g., Ogura and

Ishida 1995). Tagging and transplantation experiments on Atlantic salmon (Salmo salar)

indicate that offshore patterns of migration and orientation of salmonids at sea are stockspecific traits (Kallio-Nyberg and Ikonen 1992, Hansen et al. 1993). Direction of homeward

migration from offshore waters involves an inherited crude compass sense of direction

(Hansen et al. 1993). Kallio-Nyberg and Ikonen (1992) hypothesized that stock-specific

ocean feeding migration patterns result from natural selection of fish having the shortest

possible route to sufficiently good feeding areas for growth and reproduction, and that intrastock variation in these patterns is related to biological and environmental factors. Magnetite

crystals in the brain tissues of salmon may provide an internal compass needle that aligns

with the earth’s magnetic field (e.g., Mann et al. 1988) or, as in pied flycatchers (Ficedula

hypoleuca), geomagnetically controlled melatonin may transmit genetically encoded

orientational data (Schneider et al. 1994). As in loggerhead sea turtles (Caretta caretta; Light

et al. 1993), salmon may use inherited geomagnetic compass directions and angles of
227

Figure 1. Known ocean ranges of sockeye salmon from coastal recoveries of high seas

tagged fish (1954-95). A. Asian and North American sockeye. B. Bristol Bay

sockeye, adapted from information in Rogers (1986).

Figure 2. A conceptual model of the relationship between offshore distribution and migration patterns and natural mortality (see text for explanation).
228

inclination and anomalies of the earth’s magnetic field to navigate during their extensive

offshore migrations.

Few population-specific estimates of offshore mortality rates have been published.

Offshore mortality rates of maturing pink salmon, calculated directly from abundance

estimates of fish from the Karaginskii region of eastern Kamchatka, Russia, show

considerable annual variation (55.4-95.8%, brood years 1986-91), and in some years are

higher than coastal mortality rates of juveniles (Karpenko 1995).

In the past, the Japanese high seas salmon driftnet fisheries were a major cause of

offshore mortality. Differences in offshore distribution and migration patterns made some

populations more vulnerable to high seas fishing mortality than others. For example, tag

return data indicate that the ocean distribution of eastern Kamchatka sockeye salmon directly

overlapped the area of the pre-1978 mothership salmon driftnet fishery. Konovalov (1985)

estimated an exploitation rate of 90% by the mothership fishery on spring sockeye salmon

from Lake Azabayachi. In 1977, the U.S.S.R. 200-mile zone was closed to fishing, and after

1977 no fishing was allowed in the area north of 46°N in May, when the traditional fishery

targeted sockeye salmon. After these closures, populations of Lake Azabayachi spring

sockeye recovered rapidly (estimated abundance of spawning adults increased by 25 times

from 1977 to 1984; Konovalov 1985).

The last year of operation of the high seas salmon driftnet fisheries was 1991, and the

last year of operation of the high seas squid driftnet fisheries, which had a bycatch of salmon,

was 1992. The Convention for Conservation of Anadromous Stocks in the North Pacific

Ocean (CCAS, signed by Canada, Japan, Russia, and the United States in 1992) prohibits all

directed fishing for salmon in international waters of the North Pacific Ocean and Bering

Sea. In addition, United Nations (UN) Resolution 46/215, passed in December 1991, called

for a worldwide moratorium on all high seas large-scale driftnet fishing. Prior to the CCAS

and UN moratorium, substantial “unauthorized” salmon driftnet fishing operations were

being conducted on the high seas in violation of international treaties on salmon fishing

(Pella et al. 1993). The new international agreements, combined with the current low market

value of salmon, have effectively eliminated illegal offshore fishing for salmon.

Predation by other dominant epipelagic species (e.g., killer whales (Orcinus orca),

northern fur seals (Callorhinus ursinus), and salmon sharks (Lamna ditropis)) is likely an

important cause of natural mortality of salmon during offshore feeding and adult return

migrations. Other factors such as disease, parasites, starvation, and unusual environmental

events (e.g., El Niño) may also play a major role, but the direct causes of natural mortality in

offshore waters remain largely unknown.

Environmental changes that adversely affect complex biological processes (e.g.,

feeding, growth, maturation, run-timing, competition, predation, and disease) are likely the

major mechanisms underlying natural mortality in offshore waters. Figure 2 is a conceptual
229

model of natural mortality in offshore waters. The ellipses represent the distribution of a

discrete population at various critical life history stages. The Chinese yin-yang symbol within

the ellipses represents the dynamic interaction between environment and biological

processes. Within an area of distribution, changing environmental conditions affect various

complex biological processes, which in turn may change environmental conditions. Through

this iterative process, distributions of discrete populations expand, contract, or shift, and

offshore survival increases or decreases.

Phases in offshore distribution and migration patterns critical to survival are

1) juvenile emigration, 2) summer feeding, 3) overwintering, and 4) adult migration. In

conceptual models of migration patterns developed from historical data, offshore movement

and distribution of northeastern Pacific juvenile salmon is inferred from the distribution of

immature age 0.1 fish in the following spring. Early juvenile migrants may have moved well

offshore by January, whereas late migrants may remain for the entire winter in protected

inshore or coastal areas, and move directly offshore in the spring. Interannual variation in

timing of juvenile outmigrations and environmental conditions and, subsequently, the

distribution of juvenile salmon populations at the end of their first winter or beginning of the

first spring at sea may play a critical role in migration patterns and run-timing of returning

adults (Rogers 1986). Most offshore growth in salmon occurs during summer months.

Summer movements from one offshore feeding area to another through coastal waters may

result in increased predation or fishing mortality. Competition in offshore feeding areas may

result in decreased growth and increased age at maturity, and mortality may increase because

fish must remain at sea longer before maturing. Salmon are probably most susceptible to

predation, starvation, and disease in winter, and some populations may move from offshore

into coastal areas, where increased rates of marine mammal predation and fishing mortality

may occur. Interannual variation in timing and offshore location of adult movements may

affect location of entry into coastal areas, and, subsequently, interception in coastal fisheries

and timing of runs to river mouths (Blackbourn 1987). New offshore research should focus

on obtaining population-specific information on offshore distribution and migration patterns

and associated biological processes and environmental conditions during critical life history

phases.

Citations

Blackbourn, D. J. 1987. Sea surface temperature and pre-season prediction of return timing in

Fraser River sockeye salmon (Oncorhynchus nerka). Can. Spec. Publ. Fish. Aquat.

Sci. 96:296-306.

Burgner, R. L., J. T. Light, L. Margolis, T. Okazaki, A. Tautz, and S. Ito. 1992. Distribution

and origins of steelhead trout (Oncorhynchus mykiss) in offshore waters of the north

Pacific Ocean. Int. North Pac. Fish. Comm. Bull. 51:1-92.
230

French, R., H. Bilton, M. Osako, and A. Hartt. 1976. Distribution and origin of sockeye

salmon (Oncorhynchus nerka) in offshore waters of the North Pacific Ocean. Int.

North Pac. Fish. Comm. Bull. 34:1-113.

Godfrey, H., K. A. Henry, and S. Machidori. 1975. Distribution and abundance of coho

salmon in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm.

Bull. 31:1-80.

Hansen, L. P., N. Jonsson, and B. Jonsson. 1993. Oceanic migration in homing Atlantic

salmon. Anim. Behav. 45:927-941.

Kallio-Nyberg, I., and E. Ikonen. 1992. Migration pattern of two salmon stocks in the Baltic

Sea. ICES J. Mar. Sci. 49:191-198.

Karpenko, V. I. 1995. Estimates of ocean mortality of northeast Kamchatka pink salmon.

North Pac. Anad. Fish. Comm. Doc. 168:1-6. (Available from Kamchatka Research

Institute of Fisheries and Oceanography, 18 Naberezhnaya, PetropavlovskKamchatskii, Russia 683602.)

Konovalov, S. M. 1985. Scientific principles of the rational exploitation of Pacific salmon

and its basic scheme. Soviet J. Mar. Biol. 11(3):119-128.

Light, P., M. Salmon, and K. J. Lohmann. 1993. Geomagnetic orientation of loggerhead sea

turtles: Evidence for an inclination compass. J. Exp. Biol. 182:1-9.

Major, R. L., J. Ito, S. Ito, and H. Godfrey. 1978. Distribution and abundance of chinook

salmon (Oncorhynchus tshawytscha) in offshore waters of the North Pacific Ocean.

Int. North Pac. Fish. Comm. Bull. 38:1-54.

Mann, S., N. H. G. Sparks, M. M. Walker, and J. L. Kirschvink. 1988. Ultrastructure,

morphology and organization of biogenic magnetite from sockeye salmon,

Oncorhynchus nerka: Implications for magnetoreception. J. Exp. Biol. 140:35-49.

Myers, K. W., C. K. Harris, Y. Ishida, L. Margolis, and M. Ogura. 1993. Review of the

Japanese landbased driftnet salmon fishery in the western North Pacific Ocean and

the continent of origin of salmonids in this area. Int. North Pac. Fish. Comm. Bull.

52:1-86.

Neave, F., T. Yonemori, and R. G. Bakkala. 1976. Distribution and origin of chum salmon in

offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull. 35:1-

79.
231

Ogura, M., and Y. Ishida. 1995. Homing behavior and vertical movements of four species of

Pacific salmon (Oncorhynchus spp.) in the central Bering Sea. Can. J. Fish. Aquat.

Sci. 52:532-540.

Pella, J., R. Rumbaugh, L. Simon, M. Dahlberg, S. Pennoyer, and M. Rose. 1993. Incidental

and illegal catches of salmonids in North Pacific driftnet fisheries. Int. North Pac.

Fish. Comm. Bull. 53(III):325-358.

Quinn, T. P. 1991. Models of Pacific salmon orientation and navigation on the open ocean. J.

Theor. Biol. 150:539-545.

Rogers, D. E. 1986. Pacific salmon. In D.W. Hood and S. T. Zimmerman (editors), The Gulf

of Alaska, physical environment and biological resources, p. 461-476. NOAA, Ocean

Assessments Division, Alaska Office. (Available from the Nat. Tech. Info. Serv., U.S.

Dep. Commerce, Springfield, VA 22161.)

Schneider, T., P. Thalau-Hans, P. Semm, and W. Wiltschko. 1994. Melatonin is crucial for

the migratory orientation of pied flycatchers (Ficedula hypoleuca pallas). J. Exp.

Biol. 194:255-262.

Takagi, K., K. V. Aro, A. C. Hartt, and M. B. Dell. 1981. Distribution and origin of pink

salmon (O. gorbuscha) in offshore waters of the North Pacific Ocean. Int. North Pac.

Fish. Comm. Bull. 40:1-195.

Trenberth, K. E., and J. W. Hurrell. 1995. Decadal coupled atmosphere-ocean variations in

the North Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations, p. 15-24. Can. Spec. Publ. Fish. Aquat. Sci. 121.
232
233

MODELING TEMPORAL AND SPATIAL PATTERNS

OF SALMON MIGRATION, FEEDING, AND GROWTH

IN THE NORTHEAST PACIFIC OCEAN

Peter S. Rand, James P. Scandol, and Scott G. Hinch

Fisheries Centre and Westwater Research Unit

University of British Columbia

Vancouver, BC Canada V6T 1Z4

Processes of migration, growth, and survival of Pacific salmon in off-shore marine

environments are poorly understood. Because of logistical difficulties in sampling and

experimentation on the high seas, very few directed field efforts have been conducted to try

to gain insight into biological mechanisms regulating growth and survival of salmon in this

environment. Many of the measures of final ocean weight of salmon stocks from British

Columbia suggest a long-term reduction in mean size, perhaps related to climate change

(Hinch et al. 1996, Cox and Hinch in review). Many questions of critical importance both to

basic science, as well as to developing better practical management policies, need to be

addressed to gain a more comprehensive understanding of growth and survival of these and

other important stocks during their high seas life history stage.

We contend that much can be gained through reanalysis of past data bases involving

extensive biological sampling, coupled with the application of state-of-the-art approaches in

statistics, modeling, and data visualization that can offer fresh insights into spatial and

temporal patterns in the data. In this paper we describe a series of data bases that have been

developed over the past 40+ years and some preliminary results from analyses. We also

describe the development of an interactive software shell that allows users to test hypotheses

concerning migration and growth processes of salmon on the high seas. We apply the results

of the data analyses and modeling exercises to test the following hypotheses: 1) British

Columbia sockeye salmon (Oncorhynchus nerka) complete two loops around the Alaskan

Gyre as a result of simple behavioral rules of compass orientation and swim speed and

estimated off-shore current fields, 2) meso- (100-300 km) and gyre-scale (>1000 km)

patterns exist in zooplankton biomass and salmon feeding and growth that arise from

physical oceanographic processes, 3) the sharply defined southern limits of salmon biomass

is a result of a reduction in growth-rate potential across latitude, and 4) during spring of

1962, the area of highest growth rate potential for salmon can be found in the center of the

gyre, resulting from an optimal mix of prey abundance and thermal properties.

Data Sources and Analytical Methods

We compiled data on sea surface temperatures (SST, COADS database), off-shore

current fields (Thomson et al. 1994), zooplankton biomass (LeBrasseur 1965a, Brodeur and
234

Ware 1992), and salmon diets (LeBrasseur 1965b). The latter two data sets were based on

archived data records from the Pacific Biological Station at Nanaimo, British Columbia. The

period of biological sampling occurred during 1956-64. The sampling was extensive in space

(lat. 40-60°N, long. 120-160°W) and time (1957-64, all seasons). We focused data analysis

on the biological measures of prey (zooplankton) and predator (salmon) and tested for

significant spatial patterns and responses along latitudinal environmental gradients. We

expressed the diet data in terms of a measure of stomach fullness (proportion of maximum

daily ration), which accounts for body size-allometric effects on feeding rates (Hewett and

Kraft 1993). We applied Mantel’s tests (Mantel 1967) to detect spatial dependence in the

zooplankton and salmon gut fullness data, and developed correlograms using distance class

intervals to gain insight into the nature of the spatial patch structure. We also explored the

relationship between SST and latitude and these biological measures.

Patterns in Zooplankton Prey and Salmon Stomach Fullness

We found evidence of spatial patterns (i.e., data were spatially autocorrelated) in a

majority of the zooplankton biomass data sets. There appear to be two consistent scales at

which spatial dependence is evident. We detected meso- (100-300 km) and gyre-scale

(>1000 km) spatial dependence (Fig. 1). These results are consistent with the hypothesis that

meso-scale physical structure (e.g., eddies) may lead to the formation of meso-scale food

“patches,” while dominant offshore current fields within the Gulf of Alaska may provide a

physical template for the distribution of zooplankton at much larger scales of observation.

Analyses of pink (O. gorbuscha) and sockeye salmon stomach fullness during spring

and summer of 1962 indicated spatial similarities at a scale of approximately 1,200 km (Fig.

1). The presence of coherence in the data at this scale suggests that predators are responding

to the general gyre-scale patterns detected in the prey “landscape.” We also found a four- to

five-fold reduction in stomach fullness measures between approximately 9°C and 10°C SST

for sockeye salmon and between 10°C and 12°C SST for pink salmon. We also discovered a

sharp reduction in stomach contents below lat. 50°N, which was coincident with a reduction

in zooplankton biomass. We used the results of these analyses to develop temperature- and

prey-dependent foraging functions that were applied in the models described below.

Modeling Methods and Results

The model tracks individual migration and growth trajectories of salmon beginning

on 15 August in the vicinity of the Queen Charlotte Islands and is terminated 660 days later

(15 June) at predicted endpoints on the high seas. The model is individual-based (IBM) and

operates on a 5-day time step at a spatial resolution of 1° lat. by 1° long. The structure of the

migration submodel has been described elsewhere (Walter et al. in review). Algorithms to

estimate swim speed and bioenergetic losses can be found in a number of publications (e.g.,

Beauchamp et al. 1989). The model predicts ration and growth based on occupied
235

Figure 1. Correlograms describing meso- (100-300 km) and gyre- (>1000 km) scale

dependent patch structures in zooplankton biomass and pink salmon stomach

fullness during May-June 1962 in the Northeast Pacific Ocean. High positive

correlation coefficients (* = significance at P = 0.05) indicate coherence in

response variables at sampling stations separated at a given distance interval. Note

coherence in gyre scale patterns between prey biomass and predator feeding.
236

temperature and prey biomass within each cell in the spatial matrix (Fig. 2). We express

growth rates in two different ways. The first is the observed mean and range of projected

weights across all individuals in an IBM simulation. The second is the growth rate potential

(e.g., Brandt et al. 1992) for a representative 500-g sockeye salmon within each cell in the

ocean matrix given the spatial variability in SST and zooplankton biomass, which provides a

visual “snapshot” of growth conditions across the Northeast Pacific Ocean.

We tracked the migration trajectory, feeding, bioenergetics, and growth of 200

individual sockeye salmon over 660 days in the coast and high seas environments of the

Northeast Pacific Ocean. The model results suggest that salmon are more likely to complete

only one loop around the Gulf of Alaska prior to their spawning migration (Fig. 3). In order

for individuals in the model to complete two loops around the gyre, it was necessary to

invoke directed swimming behaviors that moved salmon in a direction parallel to the

dominant gyre currents. We report here the results of the IBM using the former, simpler

migration model. In the IBM simulation, variability in occupied temperatures was relatively

low, while variability in encounters with prey was highly variable (Fig. 4), resulting from the

prey patch structure defined above. Growth rate in the model appeared to conform to a

seasonal cycle, with highest rates of growth observed during the spring and summer, and

lowest growth rates during fall and winter.

We computed spatially explicit growth-rate potential for a 500-g sockeye salmon in

the Northeast Pacific Ocean during four seasons. Growth-rate potential was clearly highest

and most spatially heterogeneous during the spring (Fig. 5). The greatest potential for growth

during this season appeared to be centered in the mid- to lower-region of the Alaskan Gyre.

This central region appeared to correspond to an optimal mix of sufficient levels of prey

abundance and preferable thermal properties. A very sharp reduction in growth rate potential

is evident in the southern latitudes, where growth rate declines from a high of nearly 2%

body weight per day to -0.5% body weight per day along a transect of approximately 300 km.

This feature arises from the interaction between levels of zooplankton biomass (and related

feeding rates) and temperature-dependent metabolic demands. This may provide a plausible

hypothesis to explain the sharp “thermal” limits in the oceanic distribution of salmon as

described by Welch et al. (1995). One can also discern an area in the center of the gyre that

supports relatively high growth-rate potential for salmon, surrounded by concentric “rings” of

lower potential (Fig. 5). These general patterns in growth-rate potential emerge from the

results described above identifying the importance of prey abundance and temperature on

salmon feeding.

Discussion

The present model represents the product of collaborative efforts by physical,

biological, and fisheries oceanographers, along with expertise in computer software design

and data visualization. This effort represents a rare, successful marriage between biology and

technology, and will allow new insights into the ecology of Pacific salmon in coastal and
237

Figure 2. Diagram representing approach to modeling spatially explicit, individual-based

responses of salmon to prey and temperature in the North Pacific Ocean. The

spatial (1° lat by 1° long.) and temporal (5 day) resolution of the model was chosen

to achieve a balance between capturing relatively fine-scale biological processes

while minimizing computational burden. Prey and temperature were integrated

through foraging and bioenergetic algorithms to estimate growth potential for each

cell in the ocean matrix.
238

Figure 3. Plots of mean trajectory followed by simulated sockeye moving in accordance with

two different sets of migration rules from Aug-00 to June-02 (21.5 months).

Swimming speed was 0.3 body lengths/s in all simulations. (a) Preferred direction

northwest Aug-00 to Nov-00, random thereafter. (b) Preferred directions

northwest for Aug-00 to Nov-00, west for Dec-00 to Feb-01, south for Mar-01 to

May-01, east for June-01 to Aug-01, north Sep-01 to Nov-01 and repeat series

from Dec-00.

Figure 4. Mean (solid line) and range (dashed line) of exposure to environmental variables

and estimated salmon growth rate for 200 salmon in a modeled cohort. Top panel

is occupied temperature, middle panel is the history of exposure to prey biomass

during the simulation, and bottom panel reflects related growth response by

individuals within the population.
239

Figure 5. Spatially explicit growth rate potential for a representative 500 g sockeye salmon

across the Northeast Pacific Ocean during June 1962. Growth is in percent body

weight per day. Note region that supports high growth potential near the center of

the gyre, the concentric “rings” of poor growth potential surrounding it, and the

sharp reduction in growth potential at southern latitudes.
240

high seas environments. These efforts will culminate in explicit predictions in spatial

distribution and growth rates that can be rigorously tested with innovative field programs

employing new sampling technologies such as acoustics and smart tags (e.g., MacLennan

and Simmonds 1992, DeLong et al. 1992). Although much of what was described above

addresses issues related to growth and migration, we intend to apply the model to gain

insights into mechanisms responsible for regulating mortality, which is the explicit focus of

this scientific conference. We have begun to explore the trade-off between growth and

mortality in Pacific salmon using techniques of dynamic programming (Scandol et al. in

review). If indeed the critical period in the Pacific salmon life history is during the first

month or months at sea, we could gain insights into mechanisms of this process by

hindcasting growth conditions in past years. There is a substantial literature that supports the

notion that mortality is strongly size dependent, and hence growth conditions experienced by

juveniles during this period may serve as an accurate predictor of year-class strength. We are

presently working with Canada’s Department of Fisheries and Oceans and the Pacific

Salmon Commission to compile data sets on smolt migration timing, size distribution,

abundance, and subsequent survival rates for select salmon stocks. This information, coupled

with our simulation model, may allow us to better explain the observed variance in smolt-toadult survival.

One element shared by most conference presentations was a deep appreciation for the

variability that salmon survival exhibits in both space and time. This became clear through

comparisons of salmon survival across, for example, northern vs. southern salmon stocks,

pre- vs. post-1977 oceanographic conditions, and El Niño vs. La Niña climate scenarios. This

argues for future efforts that explicitly integrate effects of both space and time in the

analyses, to help explain changes in growth and survival of these important fish populations.

We hope the present effort can be successful at accomplishing this goal to help improve

conservation efforts and develop better policies for stock management.

Citations

Beauchamp, D. A., D. J. Stewart, and G. L. Thomas. 1989. Corroboration for a bioenergetics

model for sockeye salmon. Trans. Am. Fish. Soc. 118:597-607.

Brandt, S. B., D. M. Mason, E. V. Patrick. 1992. Spatially-explicit models of fish growth

rate. Fisheries (Bethesda) 17(2):23-31, 34-35.

Brodeur, R. D., and D. M. Ware. 1992. Long-term variability in zooplankton biomass in the

subarctic Pacific Ocean. Fish. Oceanogr. 1:32-38.

Cox, S. P., and S. G. Hinch. In review. Size at maturity of Fraser River sockeye salmon:

Interannual trends and the potential effects of temperature. Can. J. Fish. Aquat. Sci.

DeLong, R. L., B. S. Stewart, and R. D. Hill. 1992. Documenting migrations of northern

elephant seals using day length. Mar. Mammal Sci. 8:155-159.
241

Hewett, S. W., and C. E. Kraft. 1993. The relationship between growth and consumption:

Comparisons across fish populations. Trans. Am. Fish. Soc. 122:814-821.

Hinch, S. G., M. C. Healey, R. E. Diewert, K. A. Thomson, R. Hourston, M. A. Henderson,

and F. Juanes. 1996. Potential effects of climate change on marine growth and

survival of Fraser River sockeye salmon. Can. J. Fish. Aquat. Sci. 52:2651-2659.

LeBrasseur, R. J. 1965a. Biomass atlas of net zooplankton in the northeastern Pacific Ocean,

1956-1964. Fish. Res. Board Can. Manuscr. Rep. Ser. (Oceanogr. Limnol.) 201:1-

260.

LeBrasseur, R. J. 1965b. Data Record. Stomach contents of salmon from the northeastern

Pacific Ocean, 1958-64. Circular (Statistical Series), Nos. 15-23, Fish. Res. Board

Canada, Biological Station, Nanaimo, BC.

MacLennan, D. N., and E. J. Simmonds. 1992. Fisheries Acoustics. Chapman & Hall Fish

and Fisheries Series 5:1-325.

Mantel, N. 1967. The detection of disease clustering and a generalized regression approach.

Cancer Res. 27:209-220.

Scandol, J. P., P. S. Rand, F. Juanes, M. C. Healey, and L. Huato. In review. Examining

sockeye salmon growth and survival using dynamic optimisation to solve for

bioenergetic activity. Can. J. Fish. Aquat. Sci.

Thomson, K. A., W. J. Ingraham Jr., M. C. Healey, P. H. LeBlond, C. Groot, and C. G.

Healey. 1994. Computer simulations of the influence of ocean currents on Fraser

River sockeye salmon (Oncorhynchus nerka) return times. Can. J. Fish. Aquat. Sci.

51:441-449.

Walter, E. E., J. P. Scandol, and M. C. Healey. In review. Ocean migration patterns of Fraser

River sockeye salmon: A reanalysis of accepted patterns. Can. J. Fish. Aquat. Sci.

Welch, D. W., A. I. Chigirinsky, and Y. Ishida. 1995. Upper thermal limits on the oceanic

distribution of Pacific salmon (Oncorhychus spp.) in the spring. Can. J. Fish. Aquat.

Sci. 52:489-503.
242
243

PATTERNS OF COVARIATION IN COMPONENTS OF RECRUITMENT AMONG

SOCKEYE SALMON STOCKS IN BRITISH COLUMBIA AND ALASKA

Randall M. Peterman, Brian J. Pyper, Michael F. Lapointe1, and Milo D. Adkison2

School of Resource and Environmental Management

Simon Fraser University Burnaby, BC, Canada V5A 1S6

Current addresses:

1

Pacific Salmon Commission

600-1155 Robson St., Vancouver, BC, Canada V6E 1B5

2

National Biological Service

1011 East Tudor Road, Anchorage, AK 99503, U.S.A.

Interannual variability can be large for survival rate or body size of adults in stocks of

Pacific salmon (Oncorhynchus spp.). Within-stock or between-stock density-dependent

processes usually explain little of this variation, suggesting that environmental processes are

important (Peterman 1987). Our purpose was to identify patterns of covariation across years

and among salmon stocks in components of recruitment of fishable biomass, such as survival

rate and body size of adults. Such patterns can help characterize the spatial and temporal

scale over which environmental processes influence recruitment.

We explored patterns of covariation in two components of recruitment, an index of

survival rate and an index of body size of adults, across 21 sockeye salmon (O. nerka) stocks

from British Columbia (BC) (20 stocks from the Fraser River plus Skeena River, for brood

years 1948-86) and 9 sockeye salmon stocks from Bristol Bay, Alaska (brood years 1954-

83). Stocks from these two regions overlap for much of their marine life history. For each

stock, an index of survival rate was calculated to account for lognormal error structure and

correct for possible within-stock density-dependent effects. This index was the brood-year

residuals from a Ricker stock-recruitment model fit by linear regression of loge

(recruits per

spawner) vs. spawners. The index of body size was average length of female spawners by

age.

Correlation coefficients were calculated for pairwise comparisons among the 21 BC

stocks (210 possible comparisons), among the 9 Bristol Bay stocks (36 possible

comparisons), and between the BC and Bristol Bay stocks (189 possible comparisons) for a)

the survival index calculated for sub-2 returns (e.g., age 42

 and 52 fish) by brood year and b)

length data for age 42 female spawners by brood year. In addition, to determine which

lifestage, freshwater or marine, may be the largest contributor to interannual variability,

within-stock comparisons for Bristol Bay stocks were made by correlating the survival rate of

sub-2 and sub-3 returns with a) the same brood year and b) the same ocean-entry year (OEY).

For body size, these same within-stock correlations were done in addition to correlations

between sub-2 and sub-3 fish with the same return year.
244

There were large positive correlations in survival rate index among the Bristol Bay

stocks and, to a lesser extent, among the BC stocks, with a tendency toward negative

correlations between Bristol Bay and BC stocks (Fig. 1). This suggests that within each

region (i.e., Bristol Bay or BC) the interannual variability in survival rate of sockeye stocks is

influenced by common environmental processes, but that these processes are distinct for the

stocks of each region. For eight of the nine Bristol Bay stocks, the survival index of sub-2

adults was more highly correlated (average r = 0.47) with the survival index of sub-3 adults

of the same stock that had the same ocean-entry year versus adults that had the same brood

year (average r = 0.25). This indicates that the late freshwater or early marine lifestage

(shared by age groups with the same OEY) may be more important than the early freshwater

lifestage (shared by age groups with the same brood year) for determining variability in

survival rate.

Body size tended to be positively correlated among BC stocks and Bristol Bay stocks,

but there was no consistent correlation between Bristol Bay and BC stocks (Fig. 2). As with

the survival index, these results suggest that environmental processes influence the

interannual variability in body size of adult sockeye within each region, but not between

regions. For the Bristol Bay stocks, within-stock correlations of lengths of female spawners

were all positive and large between age groups that shared the same return year and OEY

(e.g., age 42 vs. 53 and 52 vs. 63, average r = 0.66). However, for age groups that shared the

same brood year and OEY but not the same return year, the correlations were considerably

weaker (e.g., 42 vs. 52, and 53 vs. 63, average r = 0.19). This suggests that the final year of

ocean residence (shared by age groups with the same return year) is the most critical period

for determining interannual variability in age-specific size of adults.

Patterns of covariation can also be examined by fitting different types of models that

include environmental effects to data for the residuals in loge(recruits/spawner) (details given

in Adkison et al. in press). For Bristol Bay sockeye salmon, the best-fit model was a one-time

shift in parameters of the Ricker stock-recruitment curve, coinciding with the rapid change in

the mid-1970s in intensity of the Aleutian low-pressure weather systems and associated

wind-driven processes (Trenberth and Hurrell 1994, Hare and Francis 1995). On average

across the nine Bristol Bay sockeye salmon stocks, the Ricker ‘a’ parameter (an index of

productivity) increased threefold between the early and late 1970s, whereas the Ricker ‘b’

parameter did not change appreciably or consistently among stocks. This increased

productivity is consistent with Brodeur and Ware’s (1992) finding that zooplankton

abundance increased between those two periods in the Gulf of Alaska.

These results suggest that large-scale environmental processes can strongly influence

survival and growth rates of sockeye salmon. Analyses of historical data as well as forecasts

by management agencies and the fishing industry must therefore take the spatial and

temporal scales of those environmental processes into account.
245

Figure 1. Frequency distributions of correlation coefficients (r) for the survival rate index

(residual from the Ricker stock-recruitment cure) among BC stocks (top panel),

Bristol Bay stocks (middle panel), and between BC and Bristol Bay stocks (bottom

panel).
246

Figure 2. Frequency distributions of correlation coefficients (r) for lengths of age 42 female

spawners among BC stocks (top panel), Bristol Bay stocks (middle panel), and

between BC and Bristol Bay stocks (bottom panel).
247

Funding was provided by grants to R. M. Peterman from the Ocean Production

Enhancement Network, one of Canada’s Networks of Centres of Excellence, and the Natural

Sciences and Engineering Research Council of Canada.

Citations

Adkison, M. D., R. M. Peterman, M. F. Lapointe, D. M. Gillis, and J. Korman. In press.

Alternative models of climatic effects on sockeye salmon (Oncorhynchus nerka)

production in Bristol Bay, Alaska, and the Fraser River, British Columbia. Fish.

Oceanogr. 5.

Brodeur, R. D., and D. M. Ware. 1992. Interannual and interdecadal changes in zooplankton

biomass in the subarctic Pacific Ocean. Fish. Oceanogr. 1:32-38.

Hare, S. R., and R. C. Francis. 1995. Climate change and salmon production in the Northeast

Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations. Can. Spec. Publ. Fish. Aquat. Sci. 121:357-372.

Peterman, R. M. 1987. Review of the components of recruitment of Pacific salmon. In M.

Dadswell, R. Klauda, C. Moffitt, R. Saunders, R. Rulifson, and J. E. Cooper (editors),

Common strategies of anadromous and catadromous fishes, p. 417-429. Am. Fish.

Soc. Symp. 1.

Trenberth, K. E., and J. W. Hurrell. 1994. Decadal atmosphere-ocean variations in the

Pacific. Climate Dynamics 9:303-319.
248
249

GROWTH AND ENERGETICS OF SALMON IN THE SEA

David W. Welch

Ocean Sciences and Productivity Division

Department of Fisheries and Oceans

Pacific Biological Station

Nanaimo, BC Canada V9R 5K6

Interest is growing in the question of whether the ocean as well as fresh water can

limit Pacific salmon (Oncorhynchus spp.) production. Both the North Pacific marine science

organization, PICES, and the North Pacific Anadromous Fish Commission (NPAFC) have on

their research agendas proposals to develop joint international efforts to try to answer this

question. It is likely that there are few more technically difficult questions to answer in

fisheries oceanography and few that are of potentially greater importance to salmonproducing countries.

The primary effects of the ocean on salmon productivity involve both growth and

survival of salmon. The decline in salmon survival in Washington and Oregon since 1977 is

probably caused by as yet poorly understood processes in the marine (as opposed to

freshwater) environment. The need to understand the causes of survival variations in fish are

apparent; however, comparatively little effort has been focused on understanding the changes

in growth that have occurred. Variation in growth has been assumed to be of relatively little

importance to the regulation of productivity in fish populations in general. Yet, body size at

maturity directly affects the meat yield of salmon and indirectly, and probably even more

important, the biological productivity: changes in fecundity, average age at maturity, and

ability to swim upriver and prepare and defend nest sites (Forbes and Peterman 1994).

Salmon are fundamentally marine animals whose reproduction is tied to fresh water.

Viewed as a whole, salmon spend most of their lives getting out of fresh water. Most species

probably do not even remain in the coastal environment for any significant time, instead

using the coastal environment as a transit zone during their passage offshore and again on the

return trip inshore to spawn.

From a Darwinian viewpoint, this behavior is interesting. It suggests that there are

great benefits to getting to the offshore pelagic zone as quickly as possible. Because our most

productive species are pink (O. gorbuscha), chum (O. keta), and sockeye (O. nerka) salmon

(which spend the smallest amount of time in coastal waters), this suggests that the offshore

open ocean is the most productive environment. However, since the productivity of the

offshore is much lower than the coastal region per unit area, salmon must move offshore to

either reduce rates of predation or increase growth rates because of density-dependent

interactions in the coastal zone, or both.
250

In the following sections, I review some of the evidence that a) salmon show sharp

thermal limits which appear to be the result of reducing their basal metabolic rates in times of

low food abundance, b) significant changes in rates of annual growth occur in the ocean,

c) density-dependent changes in growth are limited to the first and last years of life in the

ocean when salmon must pass through the coastal zone to the offshore, and d) evolutionary

selection has resulted in extremely sensitive responses by salmon to factors affecting their

growth rates in the offshore areas.

Effects of Ocean Temperature

Between 1955 and the late 1960s, Canada, Japan, and the United States mounted an

intensive ocean research program on the distribution of Pacific salmon. It was during this

time that North American scientists first discovered that salmon undertook extensive ocean

migrations and were not simply residents of the nearshore coastal zone during the marine

phase of their life history.

Although substantial effort was put into ocean surveys of salmon, there was little

evidence of strong limits to the distribution of salmon until recently. However, evidence for

quite strong thermal limits on their ocean distributions was found during a survey of salmon

distributions in the spring of 1990 (Welch et al. 1995). Based on these preliminary results,

Canada and Japan mounted a series of 11 one-month surveys in 1992 to further examine the

limits on the salmon distribution in different seasons and areas of the North Pacific. In

addition, we supplemented these surveys by combining all of the available Canadian and

U.S. salmon surveys for the 1950s and 1960s, and the more limited data collected by Canada

in the 1980s and 1990s. An extensive data set was also available from Japan, which has been

conducting substantial salmon surveys since 1972. (Surveys for prior years are available, but

they are not amenable to computer analysis.)

The geographic distribution of this data set, which comprises some 20,636

observations on ocean salmon abundance, is shown in Figure 1. At each location, the catch of

each species of salmon is recorded, along with the amount of fishing effort and a number of

oceanographic variables, chiefly sea surface temperature (SST).

Our current findings indicate that the primary control on salmon distribution is

temperature, but that the upper thermal limit varies throughout the year. To illustrate this

point, Figures 2a, 2b, and and 2c shows the distribution of log(salmon catch) against SST,

but with the catches split out in a trellis plot by five decades (rows) and four geographic

regions (columns) for three seasons of the year: winter, spring, and summer. (We actually

plot 1n(catch+1) to preserve the zeros in the log transformation.) Figures 2a, 2b, and and 2c

refers specifically to sockeye salmon, but our general findings also apply to all the other

species of Pacific salmon. Although the temperature defining the thermal limit in any given

month differs significantly between species in the spring and summer, and shows some

smaller variation between decades and areas of the ocean, the existence and remarkable

sharpness of this limit is the same in all species.
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Figure 1. The geographic distribution of 20,636 observations on abundance (catch per unit

effort) for each species of Pacific salmon (Oncorhynchus spp.). At each location,

information on temperature and a limited range of other data were collected. The

true density of the data set is not well represented in this plot because many

stations are overplotted dozens of times (from Welch, Ishida, and Nagasawa;

submitted to Science).
252

Figure 2a. A comparison of 1n(sockeye catch + 1) vs. temperature, splitting out the data by

season (winter: N,D,J,F,M; spring: A,M,J; summer: J,A,S). Note the sharpness of

the upper thermal limit on salmon abundance. In most cases the salmon density

drops by two orders of magnitude in a fraction of a degree Celsius. The

temperature defining the upper thermal limit varies throughout the year in a regular

cycle, but in all months it is well below lethal temperatures (>20°C) (Brett 1956).

(From Welch, Ishida, and Nagasawa; submitted to Science.)
253

Figure 2b. A comparison of 1n(sockeye catch + 1) vs. temperature, splitting out the data by

season (winter: N,D,J,F,M; spring: A,M,J; summer: J,A,S). Note the sharpness of

the upper thermal limit on salmon abundance. In most cases the salmon density

drops by two orders of magnitude in a fraction of a degree Celsius. The

temperature defining the upper thermal limit varies throughout the year in a regular

cycle, but in all months it is well below lethal temperatures (>20°C) (Brett 1956).

(From Welch, Ishida, and Nagasawa; submitted to Science.)
254

Figure 2c. A comparison of 1n(sockeye catch + 1) vs. temperature, splitting out the data by

season (winter: N,D,J,F,M; spring: A,M,J; summer: J,A,S). Note the sharpness of

the upper thermal limit on salmon abundance. In most cases the salmon density

drops by two orders of magnitude in a fraction of a degree Celsius. The

temperature defining the upper thermal limit varies throughout the year in a regular

cycle, but in all months it is well below lethal temperatures (>20°C) (Brett 1956).

(From Welch, Ishida, and Nagasawa; submitted to Science.)
255

With the exception of October, when we have no data, a thermal limit is evident in all

months. For the “winter” months of November through March, sockeye are confined to ocean

regions of <7°C. These thermal limits then begin to change, with the thermal limits

increasing from April through September, when they reach a maximum of about 15°C.

Thermal limits then begin to decline again until they finally reach the 7°C level by

November. Unfortunately, the paucity of data in the autumn prevents us from fully defining

how salmon respond to temperature during the fall, as their thermal limits must cycle back to

the winter temperature limits.

What is most remarkable about this extensive data set is just how sharp these thermal

limits are, particularly when we consider that the data extend over five decades and include

data from all parts of the North Pacific Ocean and the Okhotsk Sea. (Temperatures in the

Bering Sea never increased to levels of thermal limits recorded in the other regions of the

North Pacific.)

In British Columbia (BC) alone, there are approximately 3,150 genetically separate

stocks of the five most abundant species of salmon (Healey 1982). British Columbia formerly

produced about 15% of the total salmon from the North Pacific Ocean, which makes for a

rough estimate of 21,000 genetically separate salmon stocks occupying the North Pacific. As

the thermal limits are extremely sharp for all species, with abundances dropping by one to

two orders of magnitude in approximately 1°C, essentially all genetically separate stocks

must be responding to the same thermal limit—otherwise, such a sharp drop in abundance

would not be observed across so many populations. Whatever the specific causes of the

thermal limits are, their effects on productivity and survival for each species must be very

large, or such uniformity in the response to temperature would not be observed.

What is not clear is how such a sharp response can also exist if the different stocks

have different patterns of spatial distribution, since this would presumably make their thermal

limits different. Perhaps the stocks differentially distribute themselves within the salmon

distribution not only relative to temperature, but also in such a way as to minimize their

competition for food and thereby maximize their growth rates (see below), thereby

smoothing out local variation in the relative abundance of different stocks.

The sharpness of the roll-off in salmon abundance with temperature is best shown by

example (Fig. 3, from Welch et al. 1995). Applying the observed roll-off in abundance with

temperature to the observed temperature field present in the spring of 1990, all species of

salmon show extremely sharp declines in abundance with temperature. (The survey area

shown covered most of the central and southern Gulf of Alaska, out to about 300 nautical

miles west of Station Papa, or 2,000 km from east to west, and 1,300 km from north to

south.)
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Figure 3. The predicted geographic distribution of salmon in April, 1990, based on the R/V

TINRO data. Contour plots show the predicted temperature field, while the surface

plot shows the predicted mean response of salmon abundance to temperature. Fine

details in the abundance surfaces are dependent on the accuracy of the

interpolation of the temperature field (from Welch et al. 1995).
257

General circulation models of the world’s atmosphere predict that the oceans will

warm by 2°-3°C as the carbon dioxide content of the atmosphere doubles. What will happen

to the available thermal habitat (ATH) for salmon under a doubling of atmospheric CO2? The

predicted effect of this level of warming is quite surprising. The ATH is predicted to shrink

dramatically in both summer and winter (Fig. 4), raising the prospect that salmon will be

pushed out of the subarctic Pacific, increasing trophic competition and potentially reducing

growth rates. Thus, although much attention has been paid to the possibility that some stocks

of salmon near the southern end of their freshwater distribution may be disrupted (Fraser

River sockeye being a prime candidate (Levy 1992)), events happening in the marine phase

may be even more disruptive. At present, we have no evidence for BC salmon entering the

Bering Sea, apart from some stocks of chinook.

If the oceans warm past these sharply maintained thermal limits, BC, Washington,

and Oregon salmon would appear to have three choices: 1) develop (or express) the ability to

migrate into the Bering Sea (and return), 2) begin to vertically migrate to stay below the

permanent thermocline at about 100 m, or 3) simply incur the energetic or other penalties that

they now strongly avoid by remaining at higher temperatures.

We have no way of establishing at present which of these three mechanisms may

occur, but it seems safe to assume that since such behavior does not seem to occur now,

expressing this behavior in the future will have negative effects on salmon production. And

as BC salmon are distributed in the Gulf of Alaska, where there is no route into the Bering

Sea except at the farthest western extent of their distribution, it would seem reasonable that

further study of these possibilities is called for. It is also of some interest that marine survival

of Atlantic salmon (Salmo salar) has been correlated with interannual variation in the size

and position of 4°-8°C water in the North Atlantic (Friedland et al. 1993).

Thermal migrations and growth maximization in the ocean

The observed thermal limits are, however, qualitatively consistent with that predicted

by Welch et al. (1995), who suggested that salmon could maximize their growth rates by

lowering their body temperature and reducing basal metabolic rates in those seasons when

food levels are lower. By doing so, salmon increase the amount of food energy left for

growth, and thereby increase their somantic growth rates to a greater extent than would

otherwise be possible if they remained at constant temperature (Brett 1956, 1971). There is

also substantial evidence that fish placed in thermal gradients in the laboratory move to that

temperature yielding maximum growth rates (reviews by Beitinger and Fitzpatrick 1979,

Brett et al. 1969).

Unfortunately, this neat qualitative picture tends to fall apart in the details—the field

data are in some ways too good. Graphs of growth rate vs. temperature show a roughly

parabolic and symmetric response of growth to environmental temperature (Brett et al. 1969),

so a 1°C increase or decrease in temperature from that giving the maximum growth rate
258

Figure 4. A comparison of the predicted distribution of sockeye salmon under current and

future climates (December: 7°C; July: 10°C). Under a doubling of CO2

, predicted

to occur around the year 2070 if current trends continue, the distribution of Pacific

salmon is predicted to be drastically reduced, and thermal habitat in the North

Pacific Ocean virtually eliminated. The SST predictions are based on the Canadian

Climate Centre’s coupled ocean-atmosphere general climate model (Boer et al.

1992, McFarlane et al. 1992) (from Welch, Ishida, and Nagasawa; submitted to

Science).
259

should cause a similar reduction in growth rate. The response of each species of salmon to

temperature is clearly a step-function—temperature has no measurable effect on abundance

in the interior of the distribution (away from the edge), yet all individuals are stopping in a

fraction of a degree Celsius at the edge. The sharpness of the edge is inconsistent with growth

maximization, although the qualitative prediction is correct. It may be that salmon simply

distribute themselves in areas where they do not incur a growth deficit; that is, as long as

growth rate is positive, salmon forage independently of temperature. However, I think that

the key point for this workshop is that if all species and genetic populations of salmon are

responding with such exquisite sensitivity to factors affecting growth, then such factors may

play a very large role in the evolutionary biology, and therefore productivity.

Growth variations in salmon

Almost all salmon growth is completed in the ocean, and the final size of salmon at

return can be measured relatively accurately. In addition, the growth of scales leaves a

permanent record of the amount of growth achieved in different years at sea and, therefore,

allows us to partition the integrated growth of the body between years at sea. In essence,

although we do not know what the migration pathways of salmon are at sea in any detail, the

scale growth records allow us to treat salmon as biological conductivity, temperature, and

depth (CTD) sensors which go out to sea and record growth conditions in their scales. If we

cannot identify the influential oceanographic factors for growth, it seems unlikely that we

will ever be able to identify important factors for survival, given the difficulty with

accurately measuring the latter.

Figure 5 shows an idealized input-output sketch of the relationship between salmon

growth and a variety of underlying factors in the ocean, viewing the ocean as a chemostat.

Fish growth will not reach its maximum potential if food density (food available divided by

ocean volume) is insufficient to provide the maximum daily ration. If this critical level of

food is not exceeded, then the potential for the oceans to limit salmon growth exists. As the

examples shown later demonstrate, food availability in the ocean appears to be limiting

growth because there are large year-to-year variations in salmon size at maturity.

At food levels below critical, a general framework can be erected to describe how

salmon growth can be impacted. First, physical factors may change the productivity of the

oceans from year to year, changing the amount of food available. Second, if the geographic

distribution of salmon is limited, physical forcing of the southern (or northern) boundaries

can change the area available for grazing. Variation in physical variables can then impact

salmon growth by changing the amount of available habitat from year to year. Third, ocean

temperature may affect growth by increasing basal metabolic rates at higher temperatures,

resulting in less energy being available for growth. Finally, the number of salmon entering

the ocean may impact growth through competition for the available food.
260

Figure 5. The effect of the ocean on salmon growth, viewing the ocean as a chemostat.
261

All of these factors may impact growth. However, only the number of salmon

entering the ocean is amenable to human intervention (through manipulation of adult

escapement and ocean ranching), although it is an important variable. Increases in salmon

abundance by one country may reduce the growth rates of both their own and other countries’

salmon. The scientific issue is to disentangle and evaluate the relative contributions of these

variables on ocean salmon growth.

Effects on Growth

Accurate predictions of the future effect of climate warming on salmon are difficult.

One possible approach is to examine the response of salmon to changes in ocean climate

through retrospective analyses. The size of salmon at return to the coast varies substantially

between years (Ricker 1995). However, the effects of ocean climate on growth are

confounded with time because salmon spend 2 to 4 years at sea before their return, depending

upon species and life history type (Healey 1986). When is this variation in size expressed?

Measurements of annual growth rings on sockeye salmon scales archived at the

Department of Fisheries and Oceans and the Pacific Salmon Commission suggest that

substantial growth variation occurs at all ages (Welch 1994). However, in those stocks we

have examined so far, variations in the amount of salmon scale growth achieved in any 1 year

by a given fish is uncorrelated with the amount of growth observed at other ages for the same

fish (e.g., Figs. 6 and 7). Thus, there does not appear to be any evidence that consistently

faster- or slower-growing fish of a given stock occur, nor that the factors affecting scale

growth in different years are correlated—the spectrum for the ocean factors influencing scale

growth appears to be white rather than red on short-time scales.

Several general effects on scale growth do appear to be noteworthy, however. First,

long-term declining trends in scale growth appear to be largely confined to those ages when a

given life history type transits the coastal zone on its way offshore or on the return trip to

spawn. This would be consistent if it is the coastal zone that is primarily food limited, and the

recent increases in salmon abundance have resulted in increased trophic competition while in

coastal waters. Supporting this conjecture, long-term trends in scale growth appear to be

largely absent for those ages when all growth occurs in offshore regions (M2 (second marine

year) growth for age 4.2 and 5.3 sockeye, and M2 and M3 growth for age 5.2 sockeye).

Interannual Changes in Ocean Temperature Fields

As the previous section shows, there are large inter-annual changes in final body size,

suggesting that food is limiting at some point in the life history (otherwise salmon should

always grow at their maximum growth rates). These variations in growth also raise the

possibility of conducting retrospective analyses to statistically identify those oceanographic

variables that influence growth.
262

Figure 6. Variation in annual rates of marine growth by year of capture for the Early Stuart

stock of Fraser River sockeye salmon. The patter of variation at different ages is

uncorrelated.
263

Figure 7. Variation in annual rates of marine growth by year of capture for age 4.2 and 5.2

Skeena River sockeye salmon. Long-term trends toward reduced scale growth are

only evident in the first and last years of growth, when sockeye transit the coastal

zone. In intermediate years, when sockeye are distributed exclusively offshore,

long-term declines in scale growth are not evident although interannual variation in

growth does occur.
264

One such factor is the area of the North Pacific Ocean thermally available to salmon

in different years. The ATH for the Gulf of Alaska can be defined as that region of the

offshore lying north of some specified isotherm, and east of 160°W. My colleagues at the

University of British Columbia (Keith Thomson, Paul LeBlond, and Ian Jardine) and I have

begun calculating these areas, using the Comprehensive Ocean-Atmosphere Data Set

(COADS) and, in more recent years, the Advanced Very High Resolution Radiometry

(AVHRR) data base.

The early results are encouraging as they suggest that since 1948 the winter ATH has

varied by a factor of 1.5 or so, while spring and summer ATHs have varied by a maximum of

slightly more than 2 (Fig. 8). Although we have not yet begun the analysis of whether

fluctuations in ocean area in conjunction with variations in salmon abundance influence

salmon growth, this avenue seems to offer a promising approach to assessing the question of

whether or not the carrying capacity of the oceans is sufficiently limited to impact the

productivity of salmon populations.

Summary

The question of whether the North Pacific Ocean has a carrying capacity sufficiently

limited that this fact should be taken into account in our salmon management plans is still a

number of years away from being adequately answered. However, the exquisitely sharp

response of the ocean distribution of salmon to temperature, presumably related to growth,

strongly suggests that natural or artificially induced changes in the growth rates of salmon

will have important effects on their productivity and, thus, on the success of our salmon

fisheries. The changes in ocean climate that are predicted to accompany climate warming

may have massive impacts on the biology of salmon. It is important that we develop a deeper

and more quantitative understanding of how growth and survival of salmon in the ocean will

change, and to clearly define the link between these biological changes and the sustainable

productivity of the fisheries that depend on them.

Citations

Beitinger, T. L., and L. C. Fitzpatrick. 1979. Physiological and ecological correlates of

preferred temperature in fish. Am. Zool. 19:319-329.

Boer, G. J. , N. A. McFarlane, and M. Lazare. 1992. Greenhouse gas-induced climate change

simulated with the Canadian Climate Centre’s second-generation general circulation

model. J. Climate 5:1045-1077.

Brett, J. R. 1956. Some principles in the thermal requirements of fishes. Quart. Rev. Biol.

32(2):75-87.
265

Figure 8. Variation in the amount of available thermal habitat (ATH), defined as the area of

the Gulf of Alaska north of the a) 7°C, b) 10.5°C, and c) 15°C isotherms, east of

160°W, and excluding the area of the coastal zone. Large variations between years

in the amount of thermal habitat occurred, as evidenced by the difference between

the minimum and maximum areas estimated since 1948. The seasonal cycle of

thermal habitat can be reconstructed by taking the ATH for 7°C isotherm in winter,

the 10.5°C isotherm in spring, and the 15°C isotherm in summer.
266

Brett, J. R. 1971. Energetic responses of salmon to temperature: A study of some thermal

relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus

nerka). Am. Zool. 11:99-113.

Brett, J. R., J. E. Shelbourn, and C. T. Shoop. 1969. Growth rate and body composition of

fingerling sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration

size. J. Fish. Res. Board Can. 26:2363-2394.

Forbes, L. S., and R. M. Peterman. 1994. Simple size-structured models of recruitment and

harvest in Pacific salmon (Oncorhynchus spp.). Can. J. Fish. Aquat. Sci. 51:603-616.

Friedland, K. D., D. G. Reddin, and J. F. Kocik. 1993. Marine survival of North American

and European Atlantic salmon: Effects of growth and environment. ICES J. Mar. Sci.

50:481-492.

Healey, M. C. 1982. Multispecies, multistock aspects of Pacific salmon management. In M.

C. Mercer (editor), Multispecies approaches to fisheries management advice. Can.

Spec. Publ. Fish. Aquat. Sci. 59:119-126.

Healey, M. C. 1986. Optimum size and age at maturity in Pacific salmon and effects of sizeselective fisheries. In D. J. Meerburg (editor), Salmonid age at maturity. Can. Spec.

Publ. Fish. Aquat. Sci. 89:39-52.

Levy, D. A. 1992. Potential impacts of global warming on salmon production in the Fraser

River watershed. Can. Tech. Rep. Fish. Aquat. Sci. 1889:1-108.

McFarlane, N. A., G. J. Boer, J. P. Blanchet, and M. Lazare. 1992. The Canadian Climate

Centre second-generation general circulation model and its equilibrium climate. J.

Climate 5:1013-1044.

Ricker, W. E. 1995. Trends in the average size of Pacific salmon in Canadian catches. Can.

Spec. Publ. Fish. Aquat. Sci. 121:593-602.

Welch, D. W. 1994. Variation in marine growth rates of British Columbia pink and sockeye

salmon stocks. Proceedings of the Annual Meeting of the North Pacific Anadromous

Fish Commission, Vladivostok, Russia, October 1994. NPAFC Document 94:1-30.

Welch, D. W., A. I. Chigirinsky, and Y. Ishida. 1995. Upper thermal limits on the oceanic

distribution of Pacific salmon (Oncorhynchus spp.) in the spring. Can. J. Fish. Aquat.

Sci. 52:489-503.
267

Welch, D. W., Y. Ishida, and K. Nagasawa. In prep. Thermal limits and ocean migrations of

Pacific salmon: Long-term consequences of global warming. (Available from Ocean

Sciences and Productivity Division, Department of Fisheries and Oceans, Pacific

Biological Station, Nanaimo, BC, Canada V9R 5K6.)
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269

Working Groups
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271

WHAT HAVE WE LEARNED IN THE LAST DECADE?

WHAT ARE RESEARCH PRIORITIES?

W. G. Pearcy

College of Oceanic and Atmospheric Sciences

Oregon State University

Corvallis, OR 97331

The first workshop on the effects of ocean conditions on salmonid populations was

held here in Newport, Oregon 13 years ago, in November 1983, just after the biggest El Niño

of the century. The timing could not have been more appropriate because of the devastating

effects of this ocean event on the survival and growth of coho (Oncorhynchus kisutch) and

chinook (O. tshawytscha) salmon off Oregon and California. Warm seas farther north during

this same period, however, were correlated with near record catches of Alaskan salmon. I

believe that 1983 was the year of a paradigm shift—ocean factors were generally recognized

as important factors to salmon survival and production.

The return of many of the participants of this first workshop (with precise homing

back to Newport) is indeed gratifying, as is the attendance of marine scientists, freshwater

fishery biologists, meteorologists, administrators, and environmentalists.

What’s New Since 1983?

First to note is the general realization that ocean conditions are indeed important. This

meeting is testimony to this recognition, and to the important progress toward understanding

the relationships between the ocean environment and salmon survival. But with that progress,

the complexity of responses, both physical and biological, in different scales of time and

space, are clearly emerging. In my opinion, major changes in our thinking over the past 10 to

15 years can be grouped into four categories: El Niños, interdecadal climate shifts,

hatcheries, and ocean carrying capacity.

El Niños

The big 1982-83 El Niño event had pronounced effects on salmon growth and

survival as well as the species composition of zooplankton and of nektonic competitors and

predators of salmon in coastal waters (Pearcy 1992). Since the late 1970s, the Southern

Oscillation Index has remained low for an unprecedented duration, culminating in the

prolonged 1991-95 El Niño period (Trenberth and Hurrell 1995; Hargreaves, Beamish, and

Neville this volume) which coincided with the continued decline of some southern stocks in

the 1990s.
272

Interdecadal climate shifts

Although poor ocean conditions are often blamed on El Niños, we now realize the

significance of interdecadal changes in climatic forcing. Progress on these regime shifts has

been impressive since 1983. Papers by McLain (1984), Rogers (1984), and Chelton (1984)

presented at the first workshop identified the abrupt change in ocean temperatures that

occurred during the late 1970s, and Rogers (1984) pointed out the pronounced increase in

production of Alaskan salmon after 1976. However, the more recent papers by Brodeur and

Ware (1992), Francis and Hare (1994), Beamish and Bouillon (1995), and Hare and Francis

(1995) cogently correlated major biological and physical changes associated with this largescale regime shift, especially for the Alaskan fisheries and the Gulf of Alaska. Since the late

1970s, salmon catches in Alaska have exceeded historic highs. But for many stocks in the

southern portions of their ranges, off California and Oregon, ocean conditions have remained

generally unfavorable and populations are extremely low. The underlying mechanism for

these low-frequency shifts in climate variability remains uncertain (see Ware 1995).

Hatcheries

Hatcheries are no longer perceived as a panacea for increased production as they were

in earlier years. Now they are considered as one of the causes for declining populations of

wild stocks. In 1983, we had a working group on hatcheries and several papers were

presented on saltwater releases of salmon by authors who were employed by private salmon

ranching companies. It is revealing that there is no working group on hatcheries at this

meeting, and private salmon ranching is defunct in Oregon. The emphasis today is clearly on

restoration of declining wild stocks rather than on hatcheries.

Ocean carrying capacity

Although the oceanic or high seas carrying capacity for salmon has been evaluated

(see Pearcy 1992 for review), and both Rogers (1980) and Peterman (1984) reported negative

correlations between numbers and size of sockeye salmon, this issue has recently returned to

the fore—even more evidence is accumulating that the size of returning adult salmon has

decreased and age at maturity has increased over much of their range (e.g., Kaeriyama 1989,

Ishida et al. 1993, Helle and Hoffman 1995).

Research Priorities

Based on the recommendations of the 1983 workshop, my own personal biases, and

the results of this conference, here are some of my recommendations for future research on

ocean-salmon interactions. Many of these recommendations will be amplified in the reports

of the individual working groups.
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Three basic questions need to be addressed to reveal how ocean variability affects

growth and survival. These are the “when,” “where,” and “how” questions. When in the life

history is the most variable and highest mortality? Where—in estuarine, coastal, or oceanic

environments? How does mortality vary in time and space? And what are the mechanisms

that result in changes in growth and mortality? We need more than correlations to predict

changes in production and to assist managers. To answer these questions we need the

following types of information.

1. Better time series

We need precise and accurate time series for statistics both on salmon and on ocean

conditions. These include data on catch and escapement of adults, and numbers of smolts

entering the ocean, as well as data on size and age of both smolts and adults, in order to

a) study variations in marine survival and growth, b) compare trends in survival among

species, among stocks, and between hatchery and wild fish, and c) determine if similar trends

are related to where smolts enter the ocean or where they inhabit the ocean later in life.

We need to improve our synoptic data sets and time series for physical, atmospheric,

and biological factors that will be needed to relate salmon growth and survival to ocean

conditions.

2. Comparisons of life history strategies

More studies are required to determine the survival success of different life history

strategies within a stock (e.g., Reimers 1973). But such studies should be repeated for several

years to determine interannual variability in the survival of life history groups and how they

may relate to changing ocean conditions. Similarly, releases of smolts at different times, at

different sizes, and at different locations should be compared with relevant ocean conditions.

3. Distributions at sea

We need better information on distributions of stocks in coastal and oceanic waters,

both horizontally and vertically; how their ocean environments change over time; and how

distributions of stocks overlap. When and where and under what conditions are growth rates

suppressed? To answer these questions we need to identify fish with tags (including

acoustical and archival tags), thermal marks, scale patterns, genetic markers, etc.
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4. Partitioning survival

In my opinion, partitioning survival between freshwater and marine phases is an

extremely urgent problem. As we have seen at this workshop, climatic shifts result in wet/

cool vs. dry/warm periods that affect both the ocean and terrestrial habitats (Anderson this

volume). Although we can assume that many hatchery smolts migrate short distances to sea,

hence their post-smolt mortality is mainly in the ocean, we cannot assume this for wild

stocks. Here, freshwater conditions are much more important (Bradford this volume).

Therefore, we need to monitor numbers of wild smolts entering the ocean and the catch and

escapement of surviving adults of “indicator” stocks so that both freshwater and marine

survival rates can be estimated (similar to the long-term research at Carnation Creek). This

will provide basic information on survival rates in these two environments and will allow

evaluation of restoration efforts and recovery of depleted stocks. Estuarine mortality is

undoubtedly important for some species and stocks and also needs to be studied by serial

marking, mark and recapture, and monitoring smolts entering and leaving the estuary.

5. Experiments and modeling

We need experiments to test hypotheses of density-dependent smolt mortality in the

ocean and effects of hatchery releases on wild fish by releasing a large range in numbers of

hatchery smolts, either in different locations in the same year or large and small releases in

the same region during the same year.

Modeling can be useful in identifying critical processes that affect mortality, growth,

or distributions. Examples from this workshop are the interactions between ocean circulation

and distributions of salmon (Rand et al. this volume) and bioenergetic modeling (Brodeur

this volume).

6. Process studies at sea

To understand mechanisms, we must go to sea. Integrated research on salmonid

ecosystems is needed in both coastal and oceanic waters. In 1983, we recommended processoriented research on a few selected stocks (Oregon Production Index (OPI) coho salmon and

Bristol Bay sockeye salmon) to elucidate mechanisms linking ocean growth and survival to

ocean conditions. Such research should include study of ocean distribution and migration,

growth, feeding ecology, potential competitors and predators, and alternative prey of

predators. Today, the only comprehensive study of the early ocean life of salmon is the SEA

program in Prince William Sound (Cooney this volume).

Predation, in my opinion, is the most likely cause of high mortality rates of juvenile

salmon at sea. Because smolts are only available to marine predators for short periods of the

year, most predators must sustain themselves on more abundant forage animals. Therefore,
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the availability of alternate prey may be important in regulating predation rates on juvenile

salmon. When usually abundant forage is not available due to unfavorable ocean conditions,

predation on juvenile salmon is probably intensified. Moreover, as we have heard at this

meeting, migratory piscivorous fishes such as mackerel and Pacific hake (Merluccius

productus) may migrate into coastal waters in large numbers and prey on salmon smolts

during warm ocean conditions (Hargreaves this volume).

7. Ocean monitoring

One of the strong recommendations from 1983 was for long-term monitoring of the

coastal ocean so that ocean dynamics can be related to trends of salmon survival and growth.

The currently available time series from shore stations, on sea level, sea surface temperatures,

and occasionally sea surface salinity, are inadequate for understanding mechanisms

influencing survival and growth. For example, the relationship between upwelling intensity

during the summer and OPI hatchery coho salmon survival was significant and positive from

1960 to 1975 (Nickelson 1986) but was insignificant and negative after 1976 (Pearcy in

press). This difference is probably due to changes in the effectiveness of upwelling in

recharging the euphotic zone with nutrients. After 1976, a deep stratified layer of warm water

often persisted in coastal waters off southern California (Roemmich and McGowan 1995),

and probably farther north in the California Current system. We need routine cruises by

research vessels that monitor ocean conditions along predesignated transects from the coast.

Such cruises, along with data on currents, sea temperatures, and phytoplankton from satellite

measurements, drifters, and moored buoys, would provide relevant data on subsurface

oceanography, circulation dynamics, and water types, and on factors affecting plankton

productivity.

8. Basin-scale oceanography

Also needed are basin scale studies of circulation to evaluate variability in large-scale

physical forcing. The Chelton and Davis (1982) model showing that the California and

Alaska current systems are linked and out-of-phase should be tested. This is an important

concept in understanding regime shifts and inputs of subarctic waters into coastal waters (see

Parrish this volume for alternative ideas). Deployment of moored and drifting buoys, satellite

measurements, and ships of opportunity could all be used to further our knowledge of how

circulation is related to general trends of salmonid survival and abundance.

Citations

Beamish, R. J., and D. R. Bouillon. 1995. Marine fish production trends off the Pacific coast

of Canada and the United States. In R. J.Beamish (editor), Climate change and

northern fish populations, p. 585-591. Can. Spec. Publ. Fish. Aquat. Sci. 121.
276

Brodeur, R. D., and D. M. Ware. 1992. Long-term variability in zooplankton biomass in the

subarctic Pacific Ocean. Fish. Oceanogr. 1:32-38.

Chelton, D. B. 1984. Short-term climatic variability in the Northeast Pacific Ocean. In W. G.

Pearcy (editor), The influence of ocean conditions on the production of salmonids in

the North Pacific, p. 87-99. Oregon Sea Grant Program, Oregon State Univ.,

Corvallis. Publ. ORESU-W-83-001.

Chelton, D. B., and R. E. Davis. 1982. Monthly mean sea level variability along the west

coast of North America. J. Phys. Oceanogr. 12:757-789.

Francis, R. C., and S. R. Hare. 1994. Decadal-scale regime shifts inthe large marine

ecosystems of the North-east Pacific: A case study for historical science. Fish.

Oceangr. 3:279-291.

Hare, S. R., and R. C. Francis. 1995. Climate change and salmon production in the Northeast

Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations, p. 357-372. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Helle, J. H., and M. S. Hoffman. 1995. Size decline and older age at maturity of two chum

salmon (Oncorhynchus keta) stocks in western North America, 1972-92. In R. J.

Beamish (editor), Climate change and northern fish populations, p. 245-260. Can.

Spec. Publ. Fish. Aquat. Sci. 121.

Ishida, Y., S. Ito, M. Kaeriyama, S. McKinnell, and K. Nagasawa. 1993. Recent changes in

the age and size of chum salmon (Oncorhynchus keta) in the North Pacific Ocean and

possible causes. Can. J. Fish. Aquat. Sci. 50:290-295

Kaeriyama, M. 1989. Aspects of salmon ranching in Japan. Physiol. Ecol. Japan. Spec. Vol.

1:625-638.

McLain, D. R. 1984. Coastal ocean warming in the Northeast Pacific, 1976-83. In W. G.

Pearcy (editor), The influence of ocean conditions on the production of salmonids in

the North Pacific, p. 61-86. Oregon Sea Grant Program, Oregon State Univ.,

Corvallis. Publ. ORESU-W-83-001.

Nickelson, T. E. 1986. Influences of upwelling, ocean temperature, and smolt abundance on

marine survival of coho salmon (Oncorhynchus kisutch) in the Oregon Production

Area. Can. J. Fish. Aquat. Sci. 43:527-535.

Pearcy, W. G. 1992. Ocean ecology of North Pacific salmonids. Washington Sea Grant

Program, University of Washington Press, Seattle, 179 p.
277

Pearcy, W. G. In press. Salmon production in changing ocean domains. In D. J. Stouder, P.

A. Bisson, and R. J. Naiman (editors), Pacific salmon and their ecosystems: Status

and future options, p. 331-354. Chapman and Itall, New York.

Peterman, R. M. 1984. Density-dependent growth in early ocean life of sockeye salmon

(Oncorhynchus nerka). Can. J. Fish. Aquat. Sci. 41:1825-1829.

Reimers, P. E. 1973. The length of residence of juvenile fall chinook salmon in Sixes River,

Oregon. Res. Rep. Fish Comm. Oregon 4(2):1-43.

Roemmich, D., and J. McGowan. 1995. Climatic warming and the decline of zooplankton in

the California Current. Science 267:1324-1326.

Rogers, D. E. 1980. Density-dependent growth of Bristol Bay sockeye salmon. In W. J.

McNeil and D. C. Himsworth (editors), Salmonid ecosystems of the North Pacific,

p. 267-283. Oregon State Univ. Press, Corvallis.

Rogers, D. E. 1984. Trends in abundance of northeastern Pacific stocks of salmon. In W. G.

Pearcy (editor), The influence of ocean conditions on the production of salmonids in

the North Pacific, p. 100-127. Oregon Sea Grant Program, Oregon State Univ.,

Corvallis. Publ. ORESU-W-83-001.

Trenberth, K. E., and J. W. Hurrell. 1995. Decadal coupled atmosphere-ocean variations in

the North Pacific Ocean. In R. J. Beamish (editor), Climate change and northern fish

populations, p.15-24. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Ware, D. M. 1995. A century and a half of change in climate of the NE Pacific. Fish.

Oceanogr. 4:267-277.
278
279

REPORT OF WORKING GROUP ON PARTITIONING SURVIVAL

Chair: Mike Bradford

Rapporteur: Colin Levings

Rationale for Attempting to Partition Survival Between

Freshwater, Estuarine, and Marine Habitats

The group concluded that a major reason for obtaining data on survival rates in the

three major habitats was to avoid “racheting to extinction.” While there appears to be

evidence for decadal-scale changes in ocean conditions and overall levels of salmon

production, it is not clear what role low frequency changes in climate have on freshwater

environments. Further, freshwater productivity may be affected by habitat disruption. Salmon

managers need information on freshwater survival to ensure that river habitats maintain the

capacity to rebuild stocks. Salmon populations are buffeted by changes in marine habitat and

fishing while at sea, and recovery from these stresses would be more difficult if the

populations were recovering from low freshwater survival as well. For example, if survival

was low in both freshwater and marine habitats simultaneously, it may be difficult to change

harvest rates fast enough to maintain a viable population. Alternatively, if salmon were

experiencing high survival rates in the sea, compensating for low survival in fresh water,

conservation of habitats might be difficult but would be essential for rebuilding efforts. It is

therefore necessary to track survival in the three major habitats simultaneously.

Research Strategies Suggested

There was some debate about the usefulness of setting up a null hypothesis for the

ecological work required, given the difficulties of designing field experiments covering

oceans and major landforms such as watersheds and estuaries. The following was suggested

as a conceptual null hypothesis: “There is no link between freshwater and ocean survival.”

It was agreed that an understanding of the roles of the three major habitat types on

salmon recruitment requires analysis of long-term series of demographic data. As a first step

it was suggested that there are some existing data sources that have not yet been fully

utilized. These include the coastwide coded-wire-tag (CWT) database, and scale archives for

sockeye salmon. A first step would be to assemble a meta-database on salmon survival that

would make information readily accessible to researchers. The databases established for

endangered species could be reviewed to avoid duplication of effort. It was recognized that

the database varies with species, sampling protocols, and geography, but it was noted that in

spite of these variations some coastwide data sets such as those for CWTs and stock

identification seem to be working.
280

While chinook salmon data for disrupted systems such as the Sacramento and

Columbia Rivers are relatively good, information from rivers and estuaries farther north, such

as the Fraser and Stikine Rivers, are poor. The northern systems offer an opportunity for

reference (or “control”) data. The information on sockeye salmon from the northern systems,

however, is good, and in fact results from these databases tend to heavily influence our

understanding of salmonid ecology in the Northeast Pacific. However, it was recommended

that investigators continue to “mine” the sockeye salmon database, including the scale

archives of the former International Pacific Salmon Fisheries Commission.

Regarding new initiatives, there was at least partial consensus that progress would be

made if research were focused on a few watersheds along the coast of the Northeast Pacific.

The emphasis of this work would be to establish long-term monitoring programs that would

allow assessment of decadal-scale processes in all environments. Research at present is not

focused enough to measure survival simultaneously in marine and freshwater habitats, and

there is a desperate need to set up coordinated studies addressing salmon survival relative to

hydrology and oceanography. A network of salmonid ecologists, oceanographers, and

hydrologists in the region might be established to move this idea along. It might be useful to

restart some of the older long-term studies on freshwater survival to speed up the process of

understanding changes in fresh water due to climate or habitat change.

Several approaches to determine survival in the three major habitat types were

discussed. It was pointed out that measuring survival rates should be viewed as the major

goal in a research program. Understanding mechanisms will be very difficult and from a

management point of view may be a secondary priority. Existing weirs and counting fences

in headwaters could be harnessed to measure survival if additional facilities were built just

above the limit of tide in the estuaries. Ocean and estuary survival could then be obtained by

subtraction. Survival in the estuary would be more difficult to obtain, but with concerted

efforts such as those of Parker (1971), the estimates could be done. The idea of tracking an

individual fish throughout its life history in freshwater, estuarine, and ocean habitats was

raised as an alternate approach to population ecology. Recent developments in telemetry may

enable such investigations.

Other possible projects could focus on habitat or landscape changes in the region, but

they should be in association with measures of survival. It was thought that investigating the

Pacific Northwest Index (sea surface temperature, rainfall, and thermocline depth) might be

extended to other coastal regions. There is also scope for development of other indices in

fresh water (e.g., snow pack) and estuaries (e.g., salt wedge penetration). Changes in the

condition of landscapes in watersheds and estuarine wetlands through time could be assessed

by analyzing historical series of aerial photos.
281

Barriers to Progress

It was concluded that there was a lack of vision for research concerning partitioning

of salmon survival in their major habitats. Terrestrial ecologists have a comprehensive

network of monitoring plants and animals and their habitats on land, but there is nothing

comparable for salmon in rivers, estuaries, and oceans. In general, funding to determine

salmon survival is spotty, unstable, and only available in crises. There is an illusion in the

public that current levels of activity are resulting in the accumulation of reliable abundance

data that can be used to monitor changes in salmon survival. It was proposed that the

involvement of nontraditional groups (National Science Foundation, schools, clubs, etc.)

might have utility in maintaining continuity in long-term monitoring programs. The reality

and need for these types of programs must be pointed out to politicians at all levels of

government, to educators, and to our friends and neighbors at the local level.

Citation

Parker, R. R. 1971. Size selective predation among juvenile salmonid fishes in a British

Columbia inlet. J. Fish. Res. Board Can. 28:1503-1570.
282
283

REPORT OF WORKING GROUP ON ESTUARINE HABITAT

PROBLEMS AND RESEARCH

Chair: Robert Emmett

Rapporteur: Bruce McCain

The estuarine work group felt that many of the research needs identified by the

Estuaries and Inlets Working Group during the 1983 meeting are still valid and perhaps even

more necessary than a decade ago. In particular, the call for long-term data sets and a

consistent research and monitoring program in estuaries in 1983 was not heeded. Participants

identified the relation between salmonid mortality and timing and duration of estuarine

residence as one of the most important unanswered questions critical to establishing the

importance of estuarine areas to the health of salmon populations. The relative lack of

knowledge about the importance of estuaries to salmonids became apparent as our group

spent a considerable amount of time discussing the need to have a document that describes

the value of estuaries to salmonids for managers and nonscientists. If managers and

governments are going to put money into estuarine research and monitoring, they need to

know how and why estuaries are an important life history stage for Pacific salmon. The role

of estuaries in the life history of the various salmonid species and stocks needs to be

described. A comprehensive review paper describing the relationship between estuaries and

salmonid life histories, similar to that of Simenstad et al. (1982), would be valuable, although

much essential information is still unavailable.

 To begin our discussion, we revisited the hypotheses identified in 1983 and reviewed

where the science has come since that time.

H1 Mortality in estuaries is size and density dependent.

We still need data on how estuarine/ocean survival varies relative to the size of smolts

and the number (densities) of smolts in estuaries. In particular, we need information on how

the structure and functions of various habitats in estuaries affects salmonid survival.

Information on dependent and independent variables, natural and anthropogenic factors

affecting mortalities, and long-term databases are unavailable for any West Coast estuary,

with the possible exception of San Francisco Bay.

A research program using salmon from hatcheries and net-pen operations (e.g.,

Youngs Bay, Columbia River estuary) focused on the effects of different smolt release

strategies (timing, size, density) relative to various estuarine habitat parameters (food,

temperature, predators, etc. ) on percent returning adults would be valuable. Of major interest

would be how specific physical and biological factors in estuaries (food, temperature,

predators, residence time, etc.) affect salmon mortalities.
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H2 Within-estuary mortality is habitat specific.

Most research related to effects of habitat-specific factors has been conducted in fresh

water, although some work has been done in Coos Bay, the Columbia River estuary, and the

Campbell River estuary. Nevertheless, these estuarine studies simply identified that estuarine

use enhanced survival but did not identify the mechanisms. The primary research issues are

the differential uses of various estuarine habitats by juvenile salmonids and the mechanisms

and functions of these uses with respect to salmonid mortalities. Research strategies

recommended by the 1983 Working Group have not been undertaken.

H3 Salmonid mortalities in estuaries are dependent upon smolt fitness.

The general feeling of the groups was that relatively more research has been done

addressing this issue than H1 and H2. A variety of measures of smoltification and

physiological status has been developed since 1983. Some physiological parameters in smolts

may also be related to critical behavior (migration rates and location, feeding habits) that

could affect survival. In addition, exposure of smolts to chemical contaminants in urban

estuaries can affect the fitness of certain juvenile salmonid species. A key question was

identified: How could fitness and physiological characteristics in hatchery reared and wild

smolts affect differential mortalities? The feeling was expressed that hatchery fish are

generally less fit than wild fish, and that the presence of hatchery fish in rivers and estuaries

could potentially reduce the fitness of co-occurring wild fish. Recent advances in blood

chemistry analysis (assays of endocrine growth factors) may assist with differentiating smolts

that are growing slowly from those that are growing rapidly, and thus be able to tell us which

smolts will survive and which estuaries/rivers are producing better smolts.

H4 Salmonid mortalities in estuaries are dependent upon the timing and duration of

estuarine residence.

This was identified as one of the most important hypotheses we discussed. Several

people expressed the opinion that natural and human-induced changes in estuaries can and

have influenced the timing and duration of estuarine residence, and that the estuarine

experience of smolts can determine ocean survival. For example, changes in regional and

coastal ocean climate and associated circulation changes can affect estuarine productivity and

availability of salmonid predators, and upwelling and freshwater inflow can affect estuarine

primary productivity and food availability. Specific questions related to this hypothesis were:

How do various salmonid species and stocks respond to various estuarine pulses in

productivity, predators, and competitors? How is the timing and duration of estuarine

residence linked to ocean conditions? How do increased salmonid densities influence timing

and duration of estuarine residence? This last question relates to the effect of hatchery

releases on estuarine use by wild salmonids.
285

It was the overall consensus of the group that much more information is needed on

this topic. Ideally, researchers would gather timing and residence-time data from a range of

estuaries, habitats, and salmon species, and from multiple years encompassing climate

variability (e.g., regime shifts) and salmonid life history durations.

H5 Size, density, condition, and time of emigration from estuaries influence coastal

and oceanic mortality rates.

This is a difficult hypothesis to test because it is difficult to distinguish between

oceanic and estuarine mortalities. Some research has been conducted, is being conducted, or

is being proposed to address this question—including the work by Reimers (1973), the

studies being conducted in the Skagit River in which smolts are being tracked from the river

to salt marshes, and possible future retrospective studies. It was generally felt that scale

studies would be valuable for determining the relative growth rates of different salmon stocks

within estuaries (some agencies and Native American tribes have extensive scale

collections).

Other Hypotheses Proposed by this Working Group

H6 Hatchery smolts influence mortalities in wild smolts.

Several factors were mentioned which could influence this hypothesis, including

competition for food, attraction of predators (e.g., mammals and birds) by major pulses of

hatchery fish, emigration timing, and disease transmission.

H7 Physical/chemical conditions in estuaries can affect the growth and survival of

migratory juvenile salmonids.

Several factors were mentioned which could influence this hypothesis, including

temperature, salinity, dissolved oxygen, flow, turbidity, and chemical contamination.

H8 Predators in estuaries can control the survival of juvenile and adult salmonids.

Several factors were mentioned which could influence this hypothesis, including the

abundance and distribution of certain species of marine mammals, birds, and fish, and the

activities of commercial and recreational human fishers.
286

H9 The presence of exotic species can affect the survival of juvenile and adult

salmonids.

Because of limited time, no defining factors were discussed by the group. However,

comparing the estuarine use and survival of salmonids in estuaries that include many exotic

species with an estuary of few exotic species may not be easy to do because nearly all

estuaries now have exotic species. Exotic species introductions into West Coast estuaries

continues to be a problem, and we may be conducting this experiment without

documentation.

H10 No single estuarine-associated factor is the dominant determinant of the

optimum health and survival of salmonids.

The large and varied life history diversity and strategies of salmonids suggest that no

single physical or biological factor may consistently determine overall salmonid survival.

Through hatchery manipulation and reductions of wild populations, overall salmonid life

history diversities have been greatly reduced. Because of this reduction, so called

“environmental bottlenecks” may now have severe consequences.

Discussion of Research Needs

There was a consensus that multidisciplinary, multiyear research programs are needed

to assess the extent and mechanisms of juvenile salmonid mortalities in estuaries and the

nearshore ocean. In particular, one major question needs to be addressed: Are physical,

chemical, and biological factors in estuaries useful predictors of the health and survival of

some life history stages of some salmonids species? Examples of suggested investigations

included:

* Determine the requirements of various life history stages of salmonid species for

various biological, chemical, and physical factors available in estuaries.

* Assess the influence of diseases on mortalities of juvenile salmonids by evaluating

relationships between disease prevalence in salmonids in estuaries and percent

returning adults to the respective rivers and hatcheries.

* Evaluate relationships between growth rates in juvenile salmonids (e.g., determined

from measurements of daily growth rings in otoliths or from scales) and percent

returning adults.

* Assess relationships among the timing of juvenile migration, the duration of estuarine

residency, and the health and survival of these juveniles.
287

These estuary studies should be performed in concert with observations of nearshore and

ocean conditions and with survival studies.

There was also a general feeling that the process of developing research strategies had

to address funding sources. Examples of important research guidelines included an

explanation of how the results would help guide management decisions about improvements

to estuaries to protect and enhance salmon stocks, address the biggest gaps in our knowledge,

and demonstrate the importance of estuaries to the recovery of depressed salmon stocks.

A number of participants expressed the feeling that estuaries are critical to the health

and survival of certain life history stages of certain salmonid species, but more information is

needed about the mechanisms. An idea was formulated to develop research programs in

small coastal estuaries, such as the estuaries of the Salmon, Alsea, Yaquina, and Siletz Rivers

in Oregon, to address some of these mechanistic questions.

Overview of Estuarine Habitat Working Group Session

Estuaries are valuable to salmonids, and research is needed to:

1. Conduct regional comparisons of watersheds and estuary linkage, and

2. Determine how estuaries and their respective salmonid stocks have been modified,

and evaluate the repercussions of these modifications.

The mechanisms for various factors in estuaries affecting the health and survival of

salmonids need to be determined. Only by conducting multiyear, multidisciplinary research,

in a variety of estuaries, can the common estuarine mechanisms controlling salmonid

estuarine/ocean survival be established.

Citations

Reimers, P. E. 1973. The length of residence of juvenile fall chinook salmon in Sixes River,

Oregon. Oregon Fish Comm. Res. Rep. 4(2):3-42.

Simenstad, C. A., K. L. Fresh, and E. O. Salo. 1982. The role of Puget Sound and

Washington coastal estuaries in the life history of Pacific salmon: an unappreciated

function. In V. S. Kennedy (editor), Estuarine comparisons, p. 343-364. Academic

Press, New York.
288
289

REPORT OF WORKING GROUP ON NEARSHORE HABITATS

Chair: W. T. Peterson

Rapporteur: R. D. Brodeur

Statement of Overall Goal

Understanding the causes of salmon declines is critical to understanding long-term

trends in salmon production, and to developing effective tools for forecasting future changes.

Goal of the Nearshore Group

Understanding factors that control mortality and growth of juvenile salmonids during

their first few months at sea is also critical.

Long-Term Trends in Salmon Production and Climate

1. The proportion of outmigrating Oregon Production Index hatchery coho salmon

smolts that return to spawn has declined from 5-10% (in 1960s and 1970s) to less

than 1% in the 1980s to present.

2. The long-term trend appears to be related to the regime-shift which took place in

1976-77; high survival was observed before the regime shift in the late 1970s and

early 1980s, low survival thereafter.

3. The proportion of coho salmon surviving to return to spawn was correlated with the

Bakun upwelling index during the 1960s and 1970s; since the early 1980s until

present, there has been no correlation with the upwelling index.

General Research Needs

* Need to understand what the Bakun upwelling index is telling us about “ocean

conditions.”

* Need to understand if wild and hatchery reared salmon have different growth and

survival rates.

* Compare growth and survival of a few index stocks of salmon in different coastal

oceanographic regions (e.g., compare juvenile salmonids that reside primarily south
290

of Cape Blanco vs. north of Cape Blanco). Also, compare adjacent stocks (e.g., Siletz,

Yaquina, Alsea) within a region to discriminate common ocean effects from natural

stream habitat effects.

* Available evidence suggests that, for Oregon Production Index (OPI) coho salmon,

much of the marine mortality occurs during the first few weeks at sea, when the

juveniles are resident nearshore and in the continental shelf waters.

General Hypotheses

H1 Mortality is due to predation by birds, mammals, and piscivorous fishes such as

mackerel and Pacific hake; recent increases in predation rate may be due to increased

abundances of predators.

H2 Mortality rates are higher during periods of poor ocean conditions (i.e., if salmon

which are just entering the sea encounter poor feeding conditions, their growth rates

may be low, their condition may be poor, and thus their small size and weakened

conditions may make them more susceptible to predation).

H3 Wild fish have higher survival rates than hatchery fish because they have higher

growth rates and are better at avoiding predators.

Most Compelling Opportunity

Beginning in 1997, all coho salmon produced in Oregon hatcheries will be marked

(adipose fin clipped). This gives us the opportunity to compare hatchery and wild fish in

estuaries and in the ocean with respect to a differential in the timing of migration to sea,

dispersal at sea, distribution and abundance, food habits, growth, and survival. In the writeup which follows, the reader should keep in mind the opportunities provided by such a

unique comparison.

Description of possible research activities

1. Calibration of Bakun upwelling index—better definition of what is meant by “good”

vs. “poor” ocean conditions

Since the climate shift in 1976-77, the Bakun upwelling index has not been a very

robust predictor of salmon survival. Although correlations between coho salmon survival and

upwelling were good for data from the pre-1976 cool regime, there is no correlation for data
291

during the present warm regime. This may be explained simply by the fact that we have not

had a summer of high upwelling since 1976, so all of the data since the late 1970s fall within

the lower quadrant (low upwelling and low survival). It may be that the signal-to-noise ratio

is now too low to permit a useful correlation. The conclusion is that it is unclear how to

interpret any correlation between salmon survival and upwelling. How does upwelling affect

salmon survival? Directly by providing a large cool-water habitat, or by setting up favorable

circulation patterns that are vital to salmon survival in some way? Indirectly by fueling

biological productivity, thus enhancing levels of prey biomass? Is there a critical interaction

between winds, circulation, upwelling and productivity in April/May when fish first go to

sea? Are such interactions more important later in the upwelling season during the period of

strong upwelling and maximum zooplankton abundance in July/August? In an interannual

context, how is the Bakun upwelling index a measure of “good” vs. “poor” ocean conditions?

Certainly a summer during which winds blew from the north every day would produce very

different biological conditions in the coastal waters off Oregon than a “normal” upwelling

season characterized by pulses in wind speed and direction.

Coastal upwelling off Oregon is characterized by active upwelling events having

northerly winds blowing for 4-10 days duration that are interrupted by periods of calm or

southerly winds. Seasonally integrated biological productivity in shelf waters is almost

certainly higher under the condition of pulsed rather than continuous upwelling. What is the

optimal set of pulsed events (e.g., 7 days upwelling, 4 days relaxed; 7 days upwelling, 7 days

relaxed . . . .)?

2. Relationships between salmon distribution, abundance, growth, and survival and the

“complexity” of coastal waters

The “complexity” of the environment may be an important feature of continental shelf

waters that is critical to salmon survival. For example, when studying a map of sea surface

temperature taken during strong upwelling, one observes mesoscale variability in the form of

fronts with complex shapes (sinuous ribbons rather than straight lines) and numerous small

eddies. The productive habitat is larger in general, with upwelled water found all over the

continental shelf and farther offshore. This complexity creates an enlarged habitat volume for

juvenile salmon with many patches where salmon may forage. During weak upwelling,

habitat is reduced in volume, there is little complexity (i.e., physical features may only

parallel the coast) and juvenile salmon may become concentrated into a smaller volume

nearshore. Since their predators may also be forced into a smaller volume, salmon may

become more susceptible to predators.

Habitat complexity is influenced by basin-scale weather and climate patterns and

freshwater discharge. Large-scale climate variations affect seasonal upwelling; duration,

intensity, and timing of freshwater discharge from the Columbia River contribute to habitat

complexity by influencing fronts.
292

The need to understand the linkages among scales was identified by several

participants. In what ways do local upwelling dynamics respond to large-scale basinwide

forcing? This is related to the problem of understanding what the upwelling index is telling

us—if the upwelling index is a function of large-scale dynamics, whereas the biological

response in nearshore waters is due to local winds, then the upwelling index may be

providing little useful information about local production.

3. Comparison of growth and survival of hatchery and wild coho

Beginning in 1997, all Oregon hatchery coho salmon will be marked (adipose fin

clipped). This gives us the opportunity to compare hatchery and wild fish in estuaries and in

the ocean with respect to studies of timing of migration to sea, distribution and abundance,

food habits, growth, and survival. This also makes possible another experiment in which

growth and survival of hatchery fish from different river systems can be compared. This

would be made possible if the otoliths of hatchery fish were thermally marked by increasing/

decreasing the temperature of hatchery pond waters for a day or two, so that a “check”

appears on the otolith. Repeated three to four times over a 2-week period, four to five checks

will be laid down. By varying the interval between checks among hatcheries, all the fish from

a hatchery would carry the same code. One could select a few river systems, mark the fish,

and compare growth/survival of fish from hatcheries from large vs. small rivers, northern vs.

southern rivers, and rivers with and without estuaries, for example.

4. Carrying capacity of the nearshore zone

When planning a comparative study of survival and growth, a key question is where

do salmon reside during their first few days at sea? If they remain in a zone very near to

shore, then a very different set of variables will operate to modulate growth and survival as

opposed to fish that immediately disperse over the entire continental shelf environment. Do

salmon seek out specific oceanographic environments (just outside the surf zone, within cool

upwelled water nearshore, mesoscale eddies or fronts, offshore in waters bordering the

Columbia River plume)? Do wild salmonids occupy different habitats than hatchery

salmonids?

5. Factors related to mortality

Who are the key predators? Are mortality rates highest during the first few days at sea

or are rates low but constant during the first few months? Studies of predation are

straightforward but will require a large effort in order to give a definite answer to the

question of who are the key predators. To obtain information on predator distribution,

biomass, and feeding rates, an ambitious field program will be needed that involves acoustic

as well as trawl surveys of potential piscivorous predators. The surveys should be conducted
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weekly during April/May to cover the first few weeks at sea, as well as at least a twicemonthly frequency during the summer months. When planning studies of predation by fishes

on juvenile salmonids, one must keep in mind that salmonids are probably rare entities within

the prey field of a Pacific hake or mackerel, for example. But, with sufficiently large sample

sizes for predators, a predation hypothesis can be evaluated. The best places to conduct such

studies may be where juvenile salmonids are most highly concentrated, such as near the

mouths of larger rivers like the Columbia or near hatcheries that are near salt water such as in

Barkeley Sound (Vancouver Island—see abstract by Hargreaves in this volume) or in Puget

Sound. In addition, bird and mammal predator surveys may be required.

6. Need to establish long-term study of a few index stocks

Given the changes in salmon survival that are associated with long-term climate

variations, we need an assessment of how key oceanographic and biological variables may

affect selected index stocks. The group agreed that new research should focus on comparing

and contrasting responses of salmonids from a few different river systems. Growth and

survival may have some stream dependency, thus there is the potential that interesting

comparisons could be made following a research plan outlined above in the section on

comparisons of stocks. Along these lines, discussion became centered upon another useful

comparison of growth and survival, that of resident stocks vs. ocean migratory stocks to sort

out mechanisms and scales of variability. Specific examples included coho salmon stocks in

Puget Sound, some of which are resident and others of which migrate into the Pacific Ocean,

returning to Puget Sound to spawn.

7. Need for coordinated efforts was stressed

The group discussed the need for a more coordinated approach to studies of

relationships between upwelling, biological productivity, ecosystem structure,

trophodynamic connection, and early life history of salmonids. The various comparisons

outlined above would be best if carried out as a long-term study in a few index streams.

Along these lines, it was recognized that we need to develop a strategy for funding

long-term studies of salmon ecology, and that the best approach may be to form an

international steering committee made of representatives from the western states (including

Alaska) and Canada at a minimum.

General Approaches

Apart from the specific process studies outlined above, the group discussed the need

for modeling studies, retrospective analyses of existing data sets, monitoring, and
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development and application of new technologies. Such work should precede process studies

because these activities would provide a richer context for hypothesis-based field process

experiments.

1. Modeling studies

Coupled physical-biological models are ideal tools to apply toward the problem of

understanding how the Bakun upwelling index is related to local production and how the

upwelling index is related to large-scale forcing. Ideally, the physical model should be a 3-D

model capable of resolving mesoscale features such as eddies, jets, and riverine plumes. The

biological component could initially be a simple NPZ model (Nutrient—Phytoplankton—

Zooplankton) imbedded in the physical model. The ultimate goal would be to build more

complex biological models that include individual-based models of salmon.

The role of predators as consumers of juvenile salmonids can be evaluated initially

through modeling. Predator-prey models should be explored that have as input data the

abundance of predators, feeding rates of predators, abundance of prey (juvenile salmonids),

and abundance of alternative prey. Initially these can be viewed as back-of-the-envelope

calculations to determine which predators appear to be the most significant. Once identified,

more careful modeling could be initiated to determine whether any top-down regulation

occurs in salmon populations.

2. Retrospective studies

Analyses of relations among salmon survival and growth and various time and space

scales of meteorological and ocean variables can be done with retrospective comparisons of

salmon survival and local forcing, survival vs. large-scale forcing, and salmon growth (using

scales) compared to local variables vs. comparisons to basin-scale variables. Large scale/

long-term retrospective studies are possible using the COADS and MOODS data sets and by

accessing climate data from the NOAA/National Climate Data Center. Oceanic and terrestrial

time series are now of sufficient length that it is possible to examine the coupled oceanicatmospheric-terrestrial system to examine, for example, effects of regime shifts on ocean

temperature, coastal weather, changes in rainfall, changes in stream flow, and salmon

survival in streams and in the ocean.

3. Monitoring

Too few coastal institutions carry out continuous routine measurements of key

oceanographic variables in continental shelf waters. Apart from long time-series of physical

parameters such as sea level, sea surface temperature, wind speed/direction, and surface

atmospheric pressure measured at buoys and shore stations, there is little information on

year-to-year or interdecadal variations in the abundance and distribution in time or space of
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plankton, small pelagic fishes, or salmon predators. We must begin to take regular

measurements of biological oceanographic variables that relate to ocean productivity, “ocean

conditions,” or salmon survival. The group agreed that such work needed to be coordinated

so that a standard set of measurements were made at common intervals along onshoreoffshore transects in key geographic regions. Transects should be located in regions that

characterize different oceanographic provinces, such as south of Cape Mendocino, between

Mendocino and Cape Blanco, off central Oregon (Newport), near the mouth of the Columbia

River, off the central Washington coast, off Vancouver Island, and off central Alaska.

Without long-term biological data it will not be possible to truly understand the biological

significance of the Bakun upwelling index, nor will it be easy to differentiate between the

terms “good ocean conditions” and “poor ocean conditions.”

4. Application of new technology

Technology exists for the mass-marking of coho salmon in hatcheries (use of rapid

changes in water temperature to produce checks on the otoliths). Such technology is used by

the Prince William Sound hatcheries to mark pink salmon. Marking of fish in this manner is

very inexpensive. The value is that it permits comparisons of survival and growth of coho

salmon as a function of river system.

The group expressed an interest in the development of improved methods of tracking

individuals (and stocks) using “smart” archival tags. These tags would record or possibly

transmit in real-time the position and depth of an individual fish through its lifetime. RNA/

DNA ratios and lipid biomarkers need to be evaluated to develop measures of relative

condition of wild and hatchery fish at sea, in relation to food supply or the origin of fish.

Coastal radar systems such as CODAR or OSCR are sufficiently developed to be

applied to long-term study of mesoscale and smaller scale (1-km resolution) variability in

upper ocean circulation patterns. With these systems it may be possible to monitor frontal

genesis so that the distributional patterns of juvenile salmon at sea can be studied in relation

to high-resolution charts of circulation and fronts. If radar data could be supplied in near realtime, sampling at sea could be coordinated with known location of fronts, eddies, and jets.
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REPORT OF WORKING GROUP ON OFFSHORE HABITAT

PROBLEMS AND RESEARCH

Chair: Katherine Myers

Rapporteur: Steve Ignell

The Offshore Habitat Working Group had an open and informative discussion about

problems and research related to oceanic growth and survival of salmon. There was general

agreement that considerably more time, effort, and thought are needed to adequately address

the objectives outlined in the workshop guidelines. The group identified and discussed some

important questions and hypotheses, which are listed below, but emphasized that these results

are not prioritized or conclusive. The group decided that its most important task during the

meeting would be to present a list of research recommendations to all attendees in the final

session prior to adjournment. The group agreed that after the meeting the Chairman would

circulate a draft of the results among the participants for review. These reviews are

incorporated into the final section of this report.

Highest Priority Questions (order of listing is not significant)

Two associated questions about distribution, migration, and life history patterns are

1. What are the distribution and migration patterns of salmon at sea? How do currents

and other physical factors influence distribution and migration patterns? (Possible

research strategies involve modeling and tagging, integrated with food studies.)

2. What triggers a change in life history stage (e.g., inshore-offshore, immaturematuring)?

Five associated questions about growth, maturation, fecundity, and survival are

3. What are the relationships between physical forcing and ocean growth and survival?

4. What causes regime-scale changes in survival?

5. What causes long-term changes in growth, maturity, and reproductive potential?

6. What is the role of the ocean in determining fecundity and lipid stores, size-at-age,

age-of-maturity, and viability of eggs?

7. How does salmon growth vary across species, space, time, etc., and what are the

causes of variability in growth of salmon?
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One question about forecasting of adult returns is

8. Can ocean-salmon-catch data be used to forecast adult returns?

Hypotheses

Four associated hypotheses related to salmon distribution and migration patterns are

H1 Physical forcing affects the oceanic distribution of salmon.

H2 Offshore migration patterns of salmon are genetically determined.

H3 Migration paths are selected to optimize growth/production, minimize energetic

losses, or, perhaps, minimize the ratio of mortality:growth.

H4 Distribution of forage affects oceanic distribution of salmon.

One hypothesis related to the underlying mechanisms of maturation is

H5 Maturation in salmon is triggered when some lipid threshold is exceeded.

Three associated hypotheses related to growth and survival are

H6 Marine survival (recruitment) is determined by events in the coastal zone.

H7 Final size is determined in the oceanic (offshore) zone.

H8 There is a positive functional relationship between growth and survival.

One hypothesis related to effects of density on growth, maturation, and reproduction

potential is:

H9 Growth, age of maturing, fecundity, and reproduction potential are density dependent

in the oceanic zone.

Three associated hypotheses related to stock-specific salmon growth are

H10 Annual stock-specific salmon growth is stationary over time.
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H11 Annual stock-specific growth varies interdecadally or shows regime-scale trends.

H12 Growth of Alaska salmonids is inversely related to growth of U.S. West Coast stocks.

Recommendations

1. An integrated, coastwide commitment to a long-term fishery-oceanographic

monitoring program in the northeastern Pacific is needed.

The working group envisioned a multidisciplinary scientific research effort,

tied to the practical need for better assessment and management of valuable marine

resources, that would benefit a variety of species, programs, and agencies. The

program would establish a sequence of monitoring lines in the North Pacific (e.g.,

p hydrologic line off Kodiak Island, Seward line, Papa line, Newport line, and

CALCOFI Line 60 off San Francisco) for collection of both surface and subsurface

data. Perhaps one vessel would be committed to a basic minimum monitoring

program to maintain these lines, but the entire package would include a mix of

surface buoys, moorings, ships, and satellites and other remote sensing devices. This

multidisciplinary effort requires a long-term commitment, and this commitment must

include all aspects of the research, not just the simple physical monitoring. The

development of this program and sampling protocols would require extensive

coordination with Global Ocean Ecosystem Dynamics Program (GLOBEC), National

Oceanic and Atmospheric Administration, Canada’s Department of Fisheries and

Oceans, and other organizations.

2. Assumptions about ocean distribution and migration patterns must be validated.

There is a need for fundamental biological information on salmon distribution

and migration patterns. New techniques (e.g., smart tags) can be used to determine

behavioral responses to temperature and other environmental factors and swimming

depths, and also as a tool to verify computer models. Stock identification using a

variety of methods (e.g., tags, electrophoresis, DNA, scales, and otolith marks) is

important to understanding the relationships among distribution, migration patterns,

and ocean survival.

3. Interaction among stocks is a key issue that needs to be investigated.

4. Research should focus on weight and energy content of salmon, not just mean lengths

or abundance.

5. There should be continued emphasis on the use of scales in studies of ocean growth.

A scale workshop coordinated by PICES (an international North Pacific marine

science organization) and NPAFC (North Pacific Anadromous Fish Commission) is

needed immediately.
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6. Better field estimates of feeding and stomach evacuation rates (24-hour sampling) and

more comprehensive studies (acoustic and net sampling) of prey species, especially

fish and squids, are needed.

There is a need to standardize gear and sampling techniques used in prey

studies. Zooplankton data are only a surrogate in areas where salmon are feeding

primarily on fish and squid. Most zooplankton gear does not catch small- to mediumsized pelagic squids and similar-sized forage fishes. There may be a need to develop

or modify existing gear (e.g., larger mouth opening for trawls) for sampling squid.

Neuston collections should be added to the standard array of forage sampling in the

areas over the continental shelf and near shore, as smaller outmigrant salmon are

surface oriented and feed on items in the neuston. The importance of neuston to

salmonids on the high seas still needs investigation.

7. There needs to be a better balance between “top-down” and “bottom-up” approaches

in the study of ocean survival.

Research should focus on predators, competitors, and disease organisms. We

should be looking at associated communities and the variability in survival due to

predation. In particular, more research on the distribution and abundance of predators

and predation rates is needed. Because of the lack of data, we may have to start with

“back-of-the-envelope” calculations. Research strategies could involve the use of

isotope analyses combined with natural chemical tracers to determine food webs.

Methods to study disease, competition, and predation need to be designed. All life

history stages need to be examined.

8. Research should focus on key stocks (e.g., Bristol Bay sockeye salmon, Prince

William Sound pink salmon, Fraser River sockeye salmon, Columbia River chinook

salmon, Oregon Production Index coho salmon, and Sacramento River chinook

salmon).

9. Working groups to coordinate research efforts should be convened more frequently

than every 13 years.

10. There is a need for coordination of acquisition and assimilation of databases, leading,

perhaps, to the development of a World Wide Web site to facilitate communication

between investigators as well as to serve as a clearinghouse of archived data useful

for the study of high-seas salmon.

The group discussed some of the databases critical for this work: 1) inshore

salmon catch and escapement data, 2) scale archives, 3) offshore catch and biological

data on both salmonids and associated species, and 4) oceanographic data.
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Post-Workshop Reviews

Peter Adams: Our principal interest has been in predator-prey studies, and my comments

deal with Recommendation 6. We have been monitoring chinook salmon stomach contents

off central California since 1980 and prey concentrations since 1983. We have been using a

24-m headrope mid-water trawl to catch forage fish and MIK nets (3-m Issac-Kidd trawls) to

catch euphausiids, both with a great deal of success. However, there is no getting around the

fundamental patchiness of both salmon feeding and prey distribution, and this requires

samples collected over a long time scale. We have found that an understanding of the feeding

dynamics and reason for the shifts in prey distributions underlay much of the changes in

salmon distribution. Finally, our neuston sampling has not been very useful in explaining

these interactions.

Dick Carlson: I have long been concerned with some of our research pursuits that seek

answers amidst many factors interacting at once, that is, a flux of conditions that are not

separable, and cannot be examined individually or experimented with except as part of a

complex. Some research programs make promises to deliver answers to questions that may

not have answers—at least none that are consistent and easily explained or understood. Some

of the questions and hypotheses we posed would be difficult to test. One area in which I see

considerable potential for developing new information is identifying ocean migration patterns

of first-year juvenile salmon. This would require sampling over the potential migration routes

often and thoroughly enough to locate stock groups of salmon that are found consistently in

certain areas or under certain conditions, and accumulating evidence for a pattern (that the

researcher defines). Separate cruises to obtain oceanographic and hydrographic information

would allow the fish sampling cruises to better focus on that activity. Recommendation 3

(interaction among stocks) also has some potential for resolution by field sampling. Capture

at sea of young salmon from stock groups found consistently together would be evidence for

interaction, and opens other avenues for investigation. Stock identification techniques would

play a major role in this effort.

Steve Ignell: I support the concept of a monitoring program (Recommendation 1), but it

needs to be tightly connected to research questions. Rather than arbitrarily set up various

monitoring lines, we need to think very carefully about how these lines will provide data to

test specific hypotheses. We also need to link the monitoring program to key index stocks. In

Recommendation 2, we need to distinguish between stock identification methods that assign

stock origin probabilities to a group of fish (GSI and scale analyses) and methods that

identify the origin of individual fish (CWT and otolith marks), as they are used to address

different research questions. The mass marking (otolith marks) of stocks of salmon in the

Gulf of Alaska offers the first good opportunity to study identifiable cohorts of different

stocks over a succession of seasons. For each stock, ocean distribution, energy stores,

growth, and maturation can be monitored in the context of biophysical variation. To expand

upon the importance of energy stores in salmon (see Recommendation 4), several lines of

research suggest that an individual’s age at maturation is determined by its energy stores,
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measured at a particular season of the year. For example, if a salmon’s lipid stores in

November exceed a “set point” of 10% whole body weight, the salmon will undergo

maturation during the succeeding year. Energy stores reflect the nutritional history of a

salmon (i.e., how well it fed during the preceding season of growth). Energy stores also

reflect the physical environmental (temperature) history, since growth is related to both ration

(amount and quality of food) and temperature.

John Karinen: In Question 3, the use of the term “physical forcing” without specification of

the range of variables or environmental conditions (e.g., site-specific and regimewide) is

inappropriate. Physical factors affecting growth and survival may range from site-specific

conditions (tidally modulated boundary effects between water masses of different

temperature, salinity, and density) to regimewide interannual, decadal, or less frequent

changes in physical conditions. Fish that are successful in finding and following food

concentrations along density gradients offshore may survive and grow faster than fish that

reside in the center of a water mass where food may not be concentrated. Regimewide

changes in physical conditions may change current patterns, temperature distribution, storm

tracks, and incidence and persistence of gyres, all of which may affect fish migration routes

and perhaps growth and survival. Hypothesis 1 should address site-specific effects rather than

regime-wide changes, which have already been shown to affect salmon migration patterns.

Do salmon key in on boundary effects and migrate along these food-rich areas? I would

change Hypothesis 3 to “Migration paths are selected to maximize survival,” as fish are,

perhaps, keying on prey abundance and avoiding predators.

Katherine Myers: Much of the difficulty that our work group had in identifying scientific

questions and translating these into testable hypotheses arises from a lack of basic

understanding of the offshore habitat and life history of Pacific salmon. Our most significant

scientific contributions in the near future will likely arise from exploratory and experimental

field research on the basic biology and ecology of salmon and associated species in offshore

waters. As stated in Recommendation 1, the need for an integrated, coastwide commitment to

a fishery-oceanographic monitoring program is closely linked to practical management and

natural resource conservation applications. The size and number of adult salmon returning to

coastal fisheries each year is largely a mystery because we do not have any information on

their oceanic growth and survival. With the end of high-seas driftnet fishing, we have a

unique opportunity to discover the natural variation in offshore growth and survival of

salmon.

Peter Rand: Many of our hypotheses are mutually exclusive, and will give rise to unique

predictions on locations and size (growth) of salmon in space and time. Through modeling

exercises, we can codify these hypotheses and make a series of predictions that can be

rigorously tested against thoughtful field sampling, ideally employing state-of-the-art

sampling technologies, such as acoustics, smart tags, and remote sensing. For example, if we

assume that salmon are “navigationally challenged” and that their movements are random,

spatial distribution can be projected solely as a consequence of dominant ocean currents. This

model can be compared to observed catch distributions. Alternatively, we can assume salmon
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are minimizing energy losses or maximizing their energy return on foraging investments,

which would lead to additional, unique predictions regarding migration behavior and

subsequent distribution that can be further tested. Modeling techniques and field sampling are

both important and operate synergistically to help move our science forward. This interplay

is particularly appropriate for offshore research because of the difficulty and expense of

carrying out exhaustive field efforts and experiments across these broad time and space

scales.

Bruce Wing: A definition of “physical forcing” (see Question 3 and Hypothesis 1) is critical

to designing observational programs. What physical features do we want the oceanographers

to monitor and investigate? Physical features such as thermal fronts, the Sitka Eddy, and river

plumes have been shown to affect the return migration routes of several species of salmon,

and there is no reason to suspect that such features do not affect outgoing migration routes.

We need to identify which features beyond and over the continental shelf are influencing

migration routes. To address Hypothesis 3, which relates to evolutionary time scales and not

to annual variability, will require a lot more basic knowledge of physical and biological

conditions than can be gathered in a short time.
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List of Attendees with Photo
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309
310
311
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Participants of the 1996 workshop on Estuarine and Ocean Survival of Northeastern Pacific

Salmon at Newport, Oregon.