Decadal changes in growth and recruitment of Pacific halibut

Decadal changes in growth and recruitment of Pacific halibut (Hippoglossus stenolepis) William G. Clark, Steven R. Hare, Ana M. Parma, Patrick J. Sullivan, and Robert J. Trumble International Pacific Halibut Commission P. O. Box 95009 Seattle, WA 98145-2009

Abstract

Since the climate regime shift of 1976-77 in the North Pacific, the individual growth of halibut (Hippoglossus stenolepis) has decreased dramatically in Alaska but not in British Columbia. Recruitment has increased dramatically in both areas. The decrease in age-specific vulnerability to commercial longline gear resulted in a persistent underestimation of incoming recruitment by the age-structured assessment method (CAGEAN) that was used to assess the stock. This problem has been corrected by adding temporal trends in growth and fishery selectivity to the assessment model. The recent sustained high level of recruitment at high levels of spawning biomass has erased the previous appearance of strong density dependence in the stock-recruitment relationship and prompted a reduction in the target full-recruitment harvest rate from 30-35% to 20-25%. The climate regime shift affected a number of other stocks of vertebrates and invertebrates in the North Pacific. While the general oceanographic changes have now been identified, the specific biological mechanisms responsible for the observed changes have not.

Introduction

The Pacific halibut (Hippoglossus stenolepis) is widely distributed in coastal waters of the North Pacific from central California to the northern Bering Sea, and on the Asian side south to Hokkaido. Aboriginal peoples in North America have fished halibut for thousands of years, and a commercial longline fishery has been conducted in U.S. and Canadian waters for more than a hundred years. Since 1923 the stock has been studied and managed by the International Pacific Halibut Commission (IPHC), making this one of the longest- and best-studied groundfish stocks in the world. Halibut assessment and management have been described by Skud (1977a), Hoag et al. (1993), and Sullivan and McCaughran (1995).

During this century there have been dramatic and persistent changes in the growth and recruitment of halibut that cannot be explained by changes in stock size. Growth was slow early in the century, rapid in the middle years, and again slow in the most recent years. The growth changes were much larger in Alaska than in British Columbia. In the case of recruitment, the pattern of alternation between periods of high and low recruitment was often represented as a cycle of about 20 yr (e.g., Parma and Deriso 1990), although there was no known reason for cyclic behavior.

Recent climatological research has provided a likely explanation of these changes as direct or indirect results of abrupt changes in the climate of the North Pacific. These changes, called “regime shifts”, occur every few decades, the most recent event having occurred in the winter of 1976/1977. This coincides closely with the recent downturn in halibut growth rates and the most recent upsurge in halibut recruitment, and with pronounced changes in the distribution and abundance of other species (Francis et al. 1998).

At this point it is clear that decadal changes in the climate of the North Pacific cause decadal changes in the life history parameters and productivity of the halibut stock, and stocks of other species. It is not at all clear what mechanisms are at work. In this paper we review the nature and timing of the changes we have observed in the halibut stock and the effect of those changes on the way that IPHC assesses and manages the stock. We also briefly summarize the current understanding of regime shifts in the North Pacific and discuss alternative hypotheses concerning the effects of climate and other factors on the halibut stock.

Changes in growth schedule and other life history parameters

Halibut on the American side of the North Pacific (Fig. 1) spawn in midwinter in the Gulf of Alaska and Bering Sea. After about six months in the plankton, the postlarvae settle out and metamorphose mostly in the western Gulf of Alaska and southeastern Bering Sea. Some of the juveniles from these nursery grounds migrate west and south to populate the central and eastern Gulf of Alaska. By age 8 the migration is complete and movement thereafter is minimal except for a seasonal spawning migration from a summer feeding area on the continental shelf to a winter spawning area in deeper water on the continental slope (Skud 1977b). The halibut fishery is conducted mainly in spring and summer when the fish are on their summer feeding grounds.

Owing to the size selectivity of longline gear, hardly any fish below a length of about 60 cm are caught in either survey or commercial operations. This length corresponds approximately to an age of 6 yr. The commercial fishery seeks out larger fish, and in addition has been subject to a minimum size limit of 32 in (81 cm) since 1974, so the youngest age-class to appear in any numbers in the commercial landings is age 8. The modal age in the commercial landings is usually 11 or 12 yr, and nearly all of the landings consist of fish 8-20 years old. Females are substantially larger than males (on average) at each age. Fish are eviscerated at sea, so the sex of the fish in the commercial landings cannot be determined.

The most useful data on the growth of halibut come from systematic longline surveys that have been conducted by IPHC from time to time since the mid-1960s, mostly in northern British Columbia (IPHC Area 2B) and around Kodiak Island (IPHC Area 3A; see Fig. 1). Additional useful data are available from research charters conducted for other purposes in 1988 and 1989. The average size at age in survey catches is of course affected by the size selectivity of longline gear, but changes over time in average size at age in survey catches reflect changes in growth. The sex of all the fish in survey catches is recorded, so the effect of sexual dimorphism can be excluded.

Between the mid-1970s and the mid-1990s, the growth of halibut in Alaska decreased dramatically (Fig. 2, upper graphs). A similar but smaller change occurred in British Columbia (Fig. 2, lower graphs). In the mid-1970s, halibut grew faster and larger in Alaska than in British Columbia; at present there is hardly any difference.

Data from research cruises in the first half of this century indicate conditions in the 1920s and 1930s very similar to those at present, with much lower growth rates than in the middle of the century and no difference in size at age between Alaska and British Columbia. These earlier data are not strictly comparable to recent setline survey data, in that they were collected on tagging trips in the winter rather than on systematic surveys in the summer. Nevertheless, the changes in both data series are so large that there is no doubt that the growth pattern of halibut in the 1920s and 1930s was very similar to the present schedule.

A detailed examination of the growth paths of individual year-classes of females in the Kodiak region over the last 20 years shows no sign of an abrupt change at the time of the 1977 climate change. Growth does not appear to have decreased substantially until the middle or late 1980s (Fig. 3), but then decreased drastically at all ages. The most recent years’ data indicate some recovery in growth rates among fish older than age 8, but the incoming 8-year-olds remain much smaller than in earlier years.

The age at which 50% of females have reached sexual maturity changed little during this period, remaining at 11-12 yr in both Alaska and British Columbia. But because of the decline in growth rates, this resulted in a large decrease in the length at 50% maturity, from 110-125 cm in the 1970s to 90-100 cm now (Fig. 4).

Effect of growth changes on the IPHC stock assessment

During the 1980s and into the 1990s, the IPHC staff estimated halibut stock size annually using the method of catch-at-age analysis called CAGEAN described by Deriso et al. (1985). This procedure consists of fitting a separable model in which fishing mortality at each age in each year is assumed to be the product of a year-specific full-recruitment fishing mortality rate and an age-specific selectivity (partial recruitment factor). The schedule of age-specific selectivities is assumed to be constant over all the years of catch-at-age and catch-per-effort data to which the model is fitted.

The vulnerability of halibut to longline gear increases with the size of the fish over a considerable range of sizes, and there is a minimum commercial size limit of 32 in (81 cm), so it could be expected that a decrease in size at age would alter the age-specific selectivity of the commercial fishery and introduce some bias into the annual stock assessment. It did.

The bias first became apparent in a retrospective examination of biomass estimates in the early 1990s, in which current estimates of biomass in a given year were compared with previous estimates of biomass in that year. Retrospective application of the CAGEAN procedure to a moving 15 yr window of data, simulating the sequence of annual assessments with no changes in the model, showed that up to the mid-1980s the initial estimate of biomass in a given year was substantially higher than the estimates obtained in subsequent assessments based on more recent data (Parma 1993). Then the pattern reversed, so that during the late 1980s and early 1990s the initial estimates were substantially lower than the subsequent estimates based on more recent data (Fig. 5). During this latter period the standard stock assessment showed a steady decline in stock size and a drastic decline in recruitment.

Retrospective patterns usually result from trends in parameters that are assumed to be constant in the model. In this case the age-specific selectivities were suspect because of the ongoing decline in size at age in the landings, but they were not the only suspect. The model was tuned to commercial catch at age and commercial catch per effort, and fishing practices were changing immediately before and after the implementation of individual quota management in Canada (1991) and Alaska (1995).

Until 1986 the Commission had conducted systematic setline surveys to provide fishery-independent data on trends in abundance, growth, and maturity. These surveys were resumed in 1993, and they confirmed the trends seen in the commercial fishery. In Alaska the survey catch rates closely matched the increasing trend of commercial catch rates, and in British Columbia indicated an even larger increase. The decline in size at age was seen to be a real change for both females and males, rather than an artifact of changed fishing practices or a changed sex ratio.

To account for the effects of the decline in size at age, the staff developed a new model that treats selectivity as size-specific rather than age-specific and allows for changes over time in the growth schedule, with resulting changes over time in the implied age-specific selectivities. Where CAGEAN estimated year-class strengths, year-specific (full-recruitment) fishing mortality rates, and constant age-specific selectivities, the new model estimates year-class strengths, year-specific fishing mortality rates, time-varying growth parameters, and size-specific selectivities for both the survey and the commercial fishery.

We initially assumed that size-specific selectivities in the survey (not the commercial fishery) had remained constant over time, and we fitted the model with a constant size-specific survey catchability and selectivity to survey and commercial catch rates, age compositions, and size-at-age distributions. Size-specific commercial catchability and selectivity were allowed to change over time, so the fits were controlled mainly by the survey data.

The fits were puzzling. IPHC uses exactly the same survey design, gear, and fishing schedule in British Columbia and Alaska, yet the model fits showed very different size-specific survey selectivities in the two areas. Survey selectivity increased from nil at 60 cm to full vulnerability at 90 cm in British Columbia, but not until 120 cm in Alaska. This suggested that selectivity was not simply a function of the gear and the growth schedule, but likely depended on some distributional or behavioral features which were more closely related to age than to size.

The size-specific model can be made to serve as an age-specific model by allowing the survey size-specific selectivities to change over time, like the commercial selectivities, but imposing a heavy penalty on any variation over time in the implied age-specific survey selectivities. This requires the survey selectivities to change over time as size-at-age changes in such a way that the implied age-specific survey selectivities remain effectively constant.

Fitting the model with the assumption of constant age-specific (rather than size-specific) survey selectivity produced similar estimates of the general trend of stock biomass in British Columbia and Alaska over the last twenty years, although the estimates of year-class strength in Alaska in recent years were substantially lower. The age-specific model fit largely eliminated the retrospective pattern that CAGEAN showed in Alaska, but not in British Columbia.

Both models produced estimates of present exploitable biomass more than double the previous CAGEAN estimates. In British Columbia, where the change in size at age was modest, the increase resulted mainly from fitting to survey rather than commercial catch rates. Survey catch rates in British Columbia in the 1990s indicated a substantially larger increase since the mid-1980s then did commercial catch rates. In Alaska, where the trends in commercial catch rates closely matched survey results but the change in size at age was dramatic, the increase resulted mainly from relaxing the assumption of a constant age-specific commercial selectivity. Recent recruitment, which had appeared to be plummeting, now appears to be soaring (Fig. 6).

At this point we cannot say which model is more appropriate. The staff’s quota recommendations for 1997 were based on the age-specific model mainly because the biomass estimates were a little lower and we preferred to err on the low side. It is somewhat ironic that with all the information about the halibut stock that is available to us, dating back to the 1920s, we are unsure of our assessment because we do not know how to interpret the survey data. In a few years, of course, when the recently recruited year-classes in Alaska have passed through the fishery, we will be better able to estimate their size and in turn find out which assumption about survey selectivity is more likely to be true.

Changes in recruitment and harvest strategy

The dramatic decline in recruitment of 8-year-olds estimated by CAGEAN during the late 1980s and 1990s coincided with a period of increasing spawning biomass during the early 1980s (Fig. 6, top panels). Opposite trends in the number of 8-yr-olds and parental biomass gave support to the hypothesis that the stock-recruitment relationship was strongly density-dependent exhibiting overcompensation.

The new stock assessment results show a very different relationship between spawning biomass and subsequent recruitment in recent years. Instead of declining, recruitment estimates for the last ten years either fluctuate without clear trend (Fig. 6, bottom panels) or they increase, depending on whether survey selectivity is assumed to be a function of age or size, respectively. In either case, recruitment appears to have fluctuated independently of stock size, at least over the observed range of spawning biomass levels.

The assessment results indicate that the number of recruits produced per unit of reproductive biomass (Fig. 7) has changed by a factor of four, showing persistent periods of low and high productivity. Peaks in productivity occur during periods of both low and high parental stock abundance and so cannot be readily explained by changes in parental biomass.

Recruitment levels estimated for 1985-1996 (year-class 1977 and subsequent) under the most conservative assumption (age-dependent selectivity) are on average about twice the average recruitment level estimated for the preceding 40 years. While the estimates for the last few years are particularly uncertain (see confidence intervals in Fig. 6), the timing of the increase in recruitment coincides with major changes in climatic regime across the North Pacific (discussed below).

IPHC sets the total allowable removals of halibut by applying a constant harvest rate to the estimate of exploitable biomass. The harvest rate is chosen by simulating stock productivity at a range of harvest rates under the operation of a range of spawner-recruit relationships consistent with historical estimates of spawning biomass and subsequent recruitment. In the past both Beverton-Holt and Ricker curves were fitted to the estimates obtained with CAGEAN, and they implied harvest rates of 0.30-0.35 to obtain maximum yield.

The recruitment estimates obtained with the new models do not indicate strong density dependence. They do indicate that the environment has played a major role in driving recruitment variation, at least within the range of stock levels observed. With this new view of historical recruitment patterns, we have considered a number of new stock-recruitment relationships for evaluating alternative harvest strategies. In all of the relationships explored, a great deal of the recruitment variability is induced by the environment, and so is not under management control. Two are described here:

(1) A Ricker (1954) model with auto-correlated environmental effects (Fig. 8a). The number of recruits at age eight is given by:

where S_t is reproductive biomass and the series of {e_t} represent environmental effects. The latter are modeled as an autoregressive process of order one:

where e_t is a normal random variable with mean 0 and variance s². The parameter r corresponds to the correlation between e _t and e _t-1. A few recruitment trajectories simulated with this model are shown in Fig. 8a.

(2) A flat model with shifts in carrying capacity (Fig. 8b). In this scenario expected recruitment increases in proportion to reproductive biomass until carrying capacity (K_i) is reached, and is constant thereafter:

Carrying capacity is affected by environmental conditions which shift between two very different regimes every 20-30 years so that alternates between two values, K1 and K2. There is additional process noise represented by the series of normally distributed random variables { }.

Both models predict that recruitment will decrease gradually as spawning biomass decreases to levels lower than the historical minimum. Predictions made about how juvenile production would change if the stock dropped to unprecedented stock levels are extremely uncertain, as they are based on an extrapolation beyond the range of historical experience.

Alternative exploitation rates were evaluated by simulating how the stock would respond to different harvest rates ranging from 0.0 to 0.50 under the operation of the new stock-recruitment relationships, and with the new, slower growth schedule. A standard age-structured model was used to simulate future trends in abundance and catches under the different harvesting regimes. Recruitment was generated according to one of the stock-recruitment models described above. The slope parameter a of the Ricker curve was set at the maximum value of in the assessment results. The alternative carrying capacities and of the flat model were set to the antilogarithms of the mean log recruitments in the periods 1943-84 and 1985-96, respectively, and a periodicity of 20 yr was used to alternate between the two. Weights at age were assumed to be fixed at the values estimated from the catch of 1996, so the possibility of future trends in growth was ignored.

Stock trajectories were simulated for 200 years, beginning at the estimated present stock level, and the performance of alternative harvest rates was evaluated on the basis of their average performance during the last 100 years of each of 500 replicates. Measures of performance were mean long-term yield, mean level of reproductive biomass, and the probability that the reproductive biomass dropped below 75,000 mt (round weight), approximately the historical minimum (attained in the mid-1930s and again in the mid-1970s), over the first 20 years of simulation. While the exploitation rate that resulted in maximum long-term yield differed for the two models considered (0.23 compared to 0.33), a range of harvest rates between 0.20 and 0.30 resulted in average yields that were within 10% of the respective maxima in both cases (Fig. 9). Even under a very optimistic scenario in which recruitment remains at the high level indicated by the last 11 estimates (i.e. a flat stock-recruitment model with carrying capacity stable at the most productive level), yields produced under a 0.25 harvest rate were only 17% lower than the maximum possible yield (obtained with a harvest rate close to 0.50).

Long-term average reproductive biomass for harvest rates between 0.20 and 0.25 ranged between 120,000 mt and 160,000 mt, well above the historical minimum (Fig. 9). Minimum levels of reproductive biomass attained in the simulated trajectories depend on the stock-recruitment model. Under the Ricker model with autocorrelated environmental effects, the probability that the stock dropped below the historical minimum over the first 20 years of simulation was small (less than 10%) for harvest rates of 0.20 and lower, but it increased substantially when the harvest rate was raised above 0.25 (Fig 9, bottom panel). The probability of dropping below the historical minimum increased more slowly for harvest rates exceeding 0.30 under the flat model as carrying capacity could remain high for several years before switching back to the low level. If, instead, high recruitment levels were assumed for the next 20 years, this probability was close to zero. These two cases are shown by the dashed lines in Fig. 9 (bottom panel).

Although it is impossible to predict long-term average yield levels, as these will depend on future environmental conditions, results indicate that harvest rates ranging from 0.20 to 0.30 may achieve close-to-maximum yields under different hypotheses about future stock productivity (Fig. 9, top panel). Harvest rates in the range 0.20-0.25 may achieve close to maximum yields under different recruitment scenarios while having a high probability that the stock level stays within the range of historical abundance.

Concurrent climatic and ecosystem changes in the Northeast Pacific

The changes in Pacific halibut growth and recruitment that we have related took place in a biological and climatic setting that has also undergone decadal scale variability this century. The nature of this variability has been characterized as abrupt shifts between different states, or regimes. The most recent regime shift in the North Pacific occurred in the winter of 1976-77 (Miller et al. 1994). Several investigators have speculated that the 1976-77 regime shift is but the most recent in a succession of events (Francis and Hare 1994, Hare and Francis 1995, Ware 1995, Hare 1996, Mantua et al. 1997, Minobe 1997, Francis et al. 1998). In the 20th century, it has been proposed that four distinct climatic regimes have occurred. The regimes have averaged 25-30 years in duration, with the transitions taking place in the mid-1920s, mid-1940s and mid-1970s. This climatic phenomenon has recently been termed the Pacific Decadal Oscillation (Mantua et al. 1997).

Biological changes associated (or at least coincident) with these climatic regime shifts have been spectacular. Evidence of bio-physical connections are evident throughout the North Pacific and Bering Sea ranging from the plankton to the highest trophic levels. Abrupt changes in population size following the winter of 1976-77 have been documented for primary production (Venrick et al. 1987), zooplankton (Brodeur and Ware 1992), crustacea (Otto 1990, Anderson 1991), and marine birds and mammals (Piatt and Anderson 1996, Merrick et al. 1997). Alaska salmon populations have shown perhaps the best documented response to North Pacific climate regime shifts (Beamish and Bouillon 1993, Francis and Hare 1994, Bigler et al. 1996). An extensive summary of North Pacific ecosystem response to interdecadal climate variability is contained in Francis et al. (1998).

Many species of demersal and pelagic fish experienced exceptionally strong year classes from 1976 to 1978 (Beamish 1993). High survival apparently occurred in response to improved ocean productivity associated with changes in the intensity of the Aleutian Low. Strong year classes and increased productivity occurred all along the northeast Pacific from California into the Bering Sea. Beamish speculated that the 1976-77 climate event influenced productivity in the California Current through changes in upwelling, and in the North Pacific through climate changes.

Hollowed and Wooster (1992; 1995) evaluated recruitment patterns and ocean conditions over a longer time period, primarily from the 1950s into the 1980s. They identified synchronous strong year classes of northeast Pacific groundfish, and attempted to associate environmental conditions with the strong year classes. Alternating warm and cool periods of sea surface temperature, averaging about a decade in duration, have occurred at least since 1932. These periods are much more frequent than the regime shifts that occur on a decadal scale. Synchronous strong recruitment occurred during a warm period. Not all warm periods exhibit synchronous strong year classes, and the species that contribute strong year classes vary from period to period. Warm periods may be necessary, but not sufficient, for strong year classes (Hollowed and Wooster 1995).

Northeast Pacific groundfish show varied patterns of abundance over the period for which data are available (Bakkala 1993; North Pacific Fishery Management Council 1996a,b). Major species in the Bering Sea and Gulf of Alaska showed a synchronous increase in abundance from the mid-1970s to the mid-1980s. Subsequently patterns changed. Walleye pollock (Theragra chalcogramma), the most abundant species in the northeast Pacific, is currently decreasing from the mid-1980s peak. Sablefish (Anoplopoma fimbria) in the Gulf of Alaska and Bering Sea-Aleutian Islands have decreased slightly (Gulf of Alaska) to greatly (Bering Sea). Pacific cod (Gadus macrocephalus) initially declined from the late 1980s, but a strong peak in abundance occurred around 1994.

Most major flatfish species in the Gulf of Alaska and the Bering Sea increased in concert with other groundfish from the mid-1970s to the mid-1980s, but either remained at high levels (Bering Sea yellowfin sole Limanda aspera) or continued to increase to the early 1990s (Gulf of Alaska arrowtooth flounder Atheresthes stomias, Bering Sea rock sole Lepidopsetta bilineata) (Fig. 10). Like Pacific halibut, Bering Sea rock sole and yellowfin sole and Gulf of Alaska arrowtooth flounder experienced very strong recruitment in the 1980s and into the 1990s relative to recruitment in the 1960s and early 1970s. Yellowfin sole, unique among the flatfish, experienced serious overfishing during the early 1960s but showed the same recruitment and abundance trends as most other flatfish. In contrast to halibut and other flatfish, Greenland turbot (Reinhardtius hippoglossoides) peaked in spawning biomass during the mid 1970s and recruitment was high through the middle and late 1970s. Since then, spawning biomass has declined steadily to the current level of about 15-20 % of the peak value and about a third of the earliest record (1970). Recruitment has fluctuated at low levels during the 1980s and 1990s.

Length at age for Bering Sea yellowfin sole and rock sole, two flatfish with abundance fluctuations similar to Pacific halibut, show little of the changes evident for halibut length at age (unpublished data, Alaska Fisheries Science Center, National Marine Fisheries Service, Seattle). Neither species showed any change over the 1982-1995 period of data availability (Fig. 11), while halibut growth rates dropped sharply in the late 1980s.

Discussion

The dramatic changes that we have observed in the growth and recruitment of Pacific halibut are clearly just one consequence of the most recent regime shift in the North Pacific, which has affected all components of the ecosystem directly and indirectly. One would not expect that all species, with differing life history strategies, ranges and adaptations, would have responded similarly to the regime shift of 1976-77. It is surprising, however, how pervasive the changes were at all trophic levels. Many, perhaps most, of the major populations of the northeast Pacific underwent major changes, some up and some down, following that winter.

Decadal shifts in population parameters have complicated the assessment of the halibut stock. As explained above, the change in growth and maturity schedules may or may not have altered the age-specific selectivity of IPHC setline surveys used for tuning the assessment. We will find out within a few years, and then we should be able to model survey selectivity correctly over time.

Regime shifts pose less of a problem for management, at least for the choice of a harvest strategy. A constant harvest rate strategy turns out to be very robust to changes in carrying capacity (Walters and Parma 1996), and as shown above it is possible to locate a harvest rate that performs well across a family of spawner-recruit curves of widely varying resiliency (i.e., slope at the origin). The worst problem in the area of policy evaluation is the common confounding of environmental and density-dependent effects. Environmentally driven trends in recruitment can easily appear as spurious evidence of density dependence (Parma and Deriso 1990) and lead to a poor choice of harvest rate. Nonstationarity in the stock-recruitment relationship should always be considered a possibility when evaluating alternative harvest strategies, even in the absence of clear signs of environmental effects.

While fixed harvest rate strategies have been shown to cope well with nonstationary stock-recruitment relationships, their performance may deteriorate when climatic shifts induce changes in growth as well, as in the case of Pacific halibut. Changes in size and maturity at age can strongly affect the lifetime reproductive contribution per recruit, which may require compensatory adjustments to the target harvest rate.

The most difficult challenge posed by decadal climate shifts is determining the specific biological mechanisms that produce the observed changes in a particular stock like Pacific halibut. In the case of growth, for example, the observed large reduction in growth in Alaska (and the much smaller reduction in British Columbia) could have been a direct result of higher temperatures in Alaska. Temperature has been shown to explain most of the regional and temporal variation observed in cod stocks in the North Atlantic (Brander 1995; Campana et al. 1995). The general decrease in salmon weight at age and decreased size at maturity has been attributed, directly and indirectly, to warmer temperatures in the Gulf of Alaska (Hinch et al. 1995, Cox and Hinch 1997). Other plausible causes of reduced halibut growth are intraspecific competition due to increased halibut abundance, or interspecific competition with other burgeoning flatfish populations. Since all these changes occurred at the same time, it is hard to identify what effect each had.

The performance of other flatfish stocks in Alaska argues against a strong effect of interspecific competition. While halibut growth rates have declined since the mid 1970s, the growth rates of rock sole and yellowfin sole in Alaska have not. This suggests that causes other than simple food supply are responsible for the observed growth changes. A change in the quality of prey may have occurred. While we are a long way from determining a cause of the changes in halibut growth rates, the mechanism must be consistent with increased survival of individuals, yet a slower growth for those individuals, similar to what was observed among Alaska salmon stocks.

The climate regime shift has, to date, been described in terms of processes acting at the atmosphere-ocean interface. Constructing reasonable linkages between atmospheric and oceanic processes and surface dwelling (plankton, salmon) or surface dependent (birds, mammals) animals is relatively straightforward. The link to groundfish, however, is more indirect and more difficult to investigate. Compared to the ocean’s surface, very little is known about the variability of conditions at the ocean’s bottom above the continental shelf and slope where groundfish reside. It is by no means certain that conditions at depth mirror those at the surface.

A number of climatically forced bottom up and top down mechanisms can be hypothesized to explain the observed changes in halibut biology. Teasing apart the various influences will require creative investigation. Nevertheless, there is reason for optimism. The 60+ year halibut otolith record provides a longer time series for analysis than is available for most other species. In addition, there are lengthy catch, recruitment and growth time series. Progress in the physical sciences has resulted in more comprehensive environmental databases. More sophisticated modeling and statistical analysis techniques have been pioneered and successfully applied in areas such as fisheries oceanography and ecology. Finally, and perhaps most importantly, an interdisciplinary approach to studies of population variability is becoming increasingly commonplace, bringing together the specialized disciplines of fisheries biology, oceanography, meteorology and statistics.

The very strong 1982-3 ENSO (El Nino-Southern Oscillation) event galvanized scientific investigation into the dynamics and impacts of ENSO. The study and understanding of decadal-scale climate variability is still in its infancy. In many ways, it resembles the early investigations into ENSO. At this stage, most studies are retrospective characterizations of physical variability and coincident ecosystem response. As the relationship between ENSO and the PDO becomes better understood, modeling efforts may ultimately allow us to predict decadal-scale regime shifts.

In summary, while we believe we have developed an assessment method and management strategy that are robust to environmentally driven changes in the Pacific halibut stock, understanding the reasons for those changes is nonetheless of great scientific interest. Research to this end is being conducted under the auspices of several national and international programs, including Global Ocean Ecosystem Dynamics (GLOBEC), the North Pacific Anadromous Fisheries Commission (NPAFC), and the North Pacific Marine Science Organization (PICES). In this manner, a comparative research approach is being implemented, with studies across species, regions and time periods providing the “replicate” observations needed to test hypotheses.

References

Anderson, P.J. 1991. Age, growth, and mortality of the northern shrimp Pandalus borealis in Pavlof Bay, Alaska. Fish. Bull. 89:541-553.

Bakkala, R.G. 1993. Structural and historical changes in the groundfish complex of the eastern Bering Sea. NOAA Tech. Rep. NMFS 114. U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration. 91 pp.

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 Bouillon, D.R. 1993. Pacific salmon production trends in relation to climate. Can. J. Fish. Aquat. Sci. 50: 1002-1016.

Bigler, B.S., Welch, D.W., and Helle, J.H. 1996. A review of size trends among North Pacific salmon (Oncorhynchus spp.). Can. J. Fish. Aquat. Sci. 53:455-465.

Brander, K.M. 1995. The effect of temperature on growth of Atlantic cod (Gadus morhua L.). ICES J. mar. Sci. 52:1-10.

Brodeur, R. D., and Ware, D.M. 1992. Interannual and interdecadal changes in zooplankton biomass in the subarctic Pacific Ocean. Fish. Oceanogr. 1: 32-38.

Campana, S.E., Mohn, R.K., Smith, S.J., and Chouinard, G.A. 1995. Spatial implications of a temperature-based growth model for Atlantic cod (Gadu morhua) off the eatern coast of Canada. Can. J. Fish. Aquat. Sci. 52:2445-2456.

Cox, S. P., and Hinch, S.G. 1997. Changes in size at maturity of Fraser River sockeye salmon (Oncorhynchus nerka) and associations with temperature. Can. J. Fish. Aquat. Sci. 54: 1159-1165.

Deriso, R.B., Quinn, T.J. II, and Neal, P.R. 1985. Catch-age analysis with auxiliary information. Can. J. Fish. Aquat. Sci. 42:815-824.

Francis, R. C., and Hare, S.R. 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., Hare, S.R., Hollowed, A.B., and Wooster, W.S. 1998. Effects of interdecadal climate variability on the oceanic ecosysterms of the northeast Pacific. Fish. Oceanogr. 7:1-21.

Hare, S.R. 1996. Low frequency climate variability and salmon production. Ph.D. Dissertation. Univ. of Washington, School of Fisheries. 306 pp.

Hare, S. R., and Francis, R.C. 1995. Climate change and salmon production in the Northeast Pacific Ocean, p. 357-372. In: R. J. Beamish [ed.] Climate Change and Northern Fish Populations. Can. Spec. Publ. Fish. Aquat. Sci. 121.

Hinch, S.G., Healey, M.C., Diewert, R.E., Thomson, K.A., Hourston, R.A., Henderson, M.A., and Juanes, F. 1995. Potential effects of climate change on marine growth and survival of Fraser River sockeye. Can. J. Fish. Aquat. Sci.52: 2651-2659.

Hoag, S.H., Peltonen, G.J., and Sadorus, L.L. 1993. Regulations of the Pacific halibut fishery, 1977-1992. International Pacific Halibut Commission Technical Report No. 27.

Hollowed, A. B., and Wooster, W.S. 1992. Variability of winter ocean conditions and strong year classes of Northeast Pacific groundfish. ICES mar. Sci. Symp. 195: 433-444.

Hollowed, A.B., and Wooster, W.S. 1995. Decadal-scale variations in the eastern Subarctic Pacific: 2. Response of Northeast Pacific fish stocks, pp. 373-385. In R.J. Beamish [ed.] Climate change and northern fish populations. Can. Spec. Pub. Fish. Aquat. Sci. 121.

Mantua, N. J., Hare, S.R., Zhang, Y., Wallace, J.M., and Francis, R.C. 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bull. Amer. Meteor. Soc. 78: 1069-1079.

Merrick, R.L., Chumbley, M.K., and Byrd, G.V. 1997. Diet diversity of Steller sea lions (Eumetopias jubatus) and their population decline in Alaska: a potential relationship. Can. J. Fish. Aquat. Sci. 54: 1342-1348.

Minobe, S. 1997. A 50-70 year climatic oscillation over the North Pacific and North America. Geophys. Res. Let. 24: 638-645.

North Pacific Fishery Management Council. 1996a. Stock assessment and fishery evaluation report for the groundfish resources of the Gulf of Alaska as projected for 1997. NPFMC, Anchorage, Alaska.

North Pacific Fishery Management Council. 1996b Stock assessment and fishery evaluation report for the groundfish resources of the Bering Sea as projected for 1997. NPFMC, Anchorage, Alaska.

Otto, R.S. 1990. An overview of eastern Bering Sea king and tanner crab fisheries. In: Proceedings of the International Symposium on King and Tanner Crabs, pp. 9-26. Alaska Sea Grant Report 90-04, University of Alaska Fairbanks.

Parma, A.M. 1993. Retrospective catch-at-age analysis of Pacific halibut: implications on assessment of harvesting policies, pp. 247-265. In G. Kruse, D.M. Eggers, R.J. Marasco, C. Pautzke, and T.J. Quinn II (eds.). Proceedings of the International Symposium on Management Strategies for Exploited Fish Populations. Alaska Sea Grant, Fairbanks, Alaska (AK-SG-93-02).

Parma, A.M., and Deriso, R.B. 1990. Experimental harvesting of cyclic stocks in the face of alternative recruitment hypotheses. Can. J. Fish. Aquat. Sci. 47:595-610.

Piatt, J.F., and Anderson, P. 1996. Response of common murres to the Exxon Valdez oil spill and long-term changes in the Gulf of Alaska marine ecosystem, p. 720-737. In S. D. Rice, R.B. Spies, D.A. Wolfe, B.A. Wright [eds] Proceedings of the Exxon Valdez Oil Spill Symposium, American Fisheries Society Symposium 18, Bethesda, MD, USA.

Ricker, W.E. 1954. Stock and recruitment. J. Fish. Res. Board Can. 11:559-623.

Skud, B.E. 1977a. Regulations of the Pacific halibut fishery, 1924-1976. International Pacific Halibut Commission Technical Report No. 15.

Skud, B.E. 1977b. Drift, migration, and intermingling of Pacific halibut stocks. International Pacific Halibut Commission Scientific Report No. 63.

Sullivan, P.J., and McCaughran, D.A. 1995. Pacific halibut assessment: changing strategies for changing times. In Assessment methodologies and management. Proceedings of the World Fisheries Congress, Theme 5. Edited by G.T. Sakagawa. Oxford & IBH Publishing Co., New Delhi. pp. 129-144.

Sullivan, P.J., Parma, A.M., and Clark, W.G. In press. Pacific halibut assessment: data and methods. International Pacific Halibut Commission Scientific Report 97.

Venrick, E. L., McGowan, J.A., Cayan, D.R., and Hayward, T.L. 1987. Climate and chlorophyll a: long-term trends in the central north Pacific Ocean. Science 238: 70-72.

Ware, D.M. 1995. A century and a half of change in the climate of the NE Pacific. Fish. Oceanogr. 4: 267-277.

Walters, C., and Parma, A.M. 1996. Fixed exploitation rate strategies for coping with effects of climate change. Can. J. Fish. Aquat. Sci. 53:148-158.