Abundance and Changes in Distribution, Biology, and Behavior of Capelin in Response to Cooler Waters of the 1990s

Transcription

1 Proceedings Forage Fishes in Marine Ecosystems 457 Alaska Sea Grant College Program AK-SG-97-01, 1997 Abundance and Changes in Distribution, Biology, and Behavior of Capelin in Response to Cooler Waters of the 1990s J. Carscadden and B.S. Nakashima Department of Fisheries and Oceans, Science Branch, St. John s, Newfoundland, Canada Abstract Indices of abundance for capelin in the Newfoundland area collected since the early 1980s include biomass estimates from offshore acoustic surveys, school surface area near spawning beaches from aerial surveys, and catch rates from the inshore commercial fishery. During the 1990s, the offshore acoustic estimates declined dramatically but the inshore indices remained stable. This divergence was coincident with below normal water temperatures and changes in capelin biology. The biological changes included large-scale changes in distribution and later spawning, both of which have been linked to the colder water temperatures, and smaller fish size. The dichotomy in the trends of abundance indices has never been fully reconciled. However, based on data from several sources, it appears that the acoustic surveys were underestimating the true population abundance of capelin offshore. It seems likely that the severe environmental conditions during the early 1990s were the major cause of the changes in biology and behavior of capelin, and these changes had their greatest impact on the acoustic estimates. Introduction Capelin is a short-lived, migratory, pelagic, schooling species and an important forage and commercial species in northern latitudes. This paper focuses only on capelin in the east and northeast coastal areas of Newfoundland (the stock complex in NAFO [Northwest Atlantic Fisheries Organization] Div. 2J3K3L) (Figure 1). Here, capelin grow and mature on offshore banks but migrate to Newfoundland beaches to spawn during late June and early July. Eggs develop and hatch in the gravel interstices

2 458 Carscadden & Nakashima Capelin Abundance in Cooler Waters Figure 1. Map of the northwest Atlantic Ocean showing NAFO divisions and place names mentioned in the text. of the intertidal zone but once into the pelagic environment, the larvae move out onto the offshore banks within a few weeks. Historically, only a small domestic fishery of about 25,000 tons was prosecuted, but during the early 1970s a major offshore foreign fishery developed. Catches in this fishery (Div. 2J3K3L) peaked at 246,000 tons in 1976 and declined rapidly until 1979 when these fisheries were either closed or quotas were drastically reduced. During the late 1970s, Canadians began fishing inshore in Div. 3K and Div. 3L, catching roe-bearing capelin for the Japanese market. The highest catches ranged between 79,000 and 83,000 tons during Three major research activities, namely acoustic surveys, aerial surveys, and a research logbook program, were initiated to monitor stocks. Two offshore acoustic surveys, one in Div. 3L during the spring (April- May) beginning in 1982 and one in Div. 2J3K during the fall beginning in 1981, were designed to estimate recruitment. These surveys were combined into one fall survey over the entire stock complex beginning in The aerial survey, started in 1982, provides an index of abun-

3 Forage Fishes in Marine Ecosystems 459 dance from estimates of school surface area derived from images of capelin schools immediately adjacent to spawning beaches. The research logbook program, started in 1981, entails voluntary completion of specially designed logbooks by a subsample of fishers. Fishers supply detailed information on catch and effort on a set-by-set basis. The catch rates and aerial survey index closely tracked each other during the 1980s (Carscadden et al. 1994). Since the initiation of these monitoring activities the oceanography of the area has varied, with the most dramatic change occurring in the late 1980s and 1990s when temperatures were at or near their lowest values since the 1940s (Drinkwater 1996) (Figure 2). At the same time, several biological characteristics of capelin have changed, some of which have been linked to the changes in the environment (Carscadden et al. In press, Frank et al. 1996). In addition, a great deal of difficulty has arisen in the interpretation of results of research activities designed to monitor the capelin stocks. The purposes of this paper are to document the changes in capelin biology and behavior during the period of below-normal ocean temperatures, and to show how these changes have influenced the interpretation of abundance indices. Changes in Capelin Biology and Behavior Offshore distribution During the early 1990s, the results from capelin acoustic surveys experienced two dramatic results: the biomass estimates showed significant and abrupt declines in both spring and fall surveys, and in the fall surveys the main area of distribution (albeit at much lower abundances) shifted farther south. In 1990, the highest estimated biomass, at almost 7 million tons, was recorded during the spring survey. In 1991, the biomass estimates dropped to about 100,000 tons, an unexpected result since some of the same year-classes contributed to both estimates. The survey was repeated about 1 month later with similar low results. Between the two surveys, the Russians completed an acoustic survey over roughly the same area and this estimate was also low (Bakanev 1992). The 1992 Canadian survey estimate was also low. Capelin in both the 1991 and 1992 surveys were widely scattered, although there was no obvious shift in distribution of the low biomass measured. The spring survey in Div. 3L was discontinued after 1992 in favor of an expanded fall survey in Div. 2J3K3L. During the 1980s, the biomass estimates from the fall surveys were variable and did not appear to be showing promise as reliable indicators of year-class abundance. The survey was expanded eastward in 1989 to compensate for possible incomplete coverage and was further enlarged to include Div. 3L beginning in However, since the fall of 1990, biomass estimates have remained very low. Equally dramatic was the

4 460 Carscadden & Nakashima Capelin Abundance in Cooler Waters Figure 2. Historical temperature anomalies at 0 m, 50 m, 100 m, and 175 m from Station 27 ( N, W).

5 Forage Fishes in Marine Ecosystems 461 Figure 3. Approximate distributions of maturing capelin (shaded areas) from fall capelin acoustic surveys in 1989 (left panel) and 1993 (right panel). Solid lines show approximate survey boundaries. Redrawn from Miller (1990, 1994). observation that the concentrations of capelin that contributed to the maturing biomass had shifted from Div. 2J to the southern part of Div. 3K and no concentrations of capelin were observed in Div. 2J and northern 3K. This change is illustrated in Figure 3 which shows the results from the fall acoustic surveys in 1989 and This shift in distribution was unusual based on the general patterns gleaned from previous acoustic surveys, historical commercial fishing patterns, bycatch in groundfish surveys conducted in November and December, and capelin in cod stomachs (Lilly and Davis 1993). Normally, capelin would be off the coast of Labrador in Div. 2J in late summer and early autumn, but by late autumn most would have migrated south into Div. 3K. Some capelin would, however, remain off Labrador even in November. Exceptions occurred in 1986 and 1987 when few capelin were found off Labrador in November. During (Lilly and Davis 1993; Lilly 1994, 1995) capelin bycatch and cod predation indicated that by November few capelin occurred in Div. 2J but the major concentrations were even farther south and east in Div. 3K than previously recorded, consistent with observations from the acoustic surveys. In addition, bycatch of overwin-

6 462 Carscadden & Nakashima Capelin Abundance in Cooler Waters tering capelin in shrimp fisheries in southern Div. 2J and northern Div. 3K during January-March also declined, consistent with the results from the fall acoustic and groundfish surveys (Carscadden 1996). Frank et al. (1996) recently reported increases in capelin abundance in areas where capelin are not usually common, namely eastern Scotian Shelf (Div. 4VW) and Flemish Cap (Div. 3M) (Figure 1). On the Scotian Shelf, capelin catch rates began to increase during the late 1980s, coincident with a decrease in water temperatures. In this area, it is not known whether the increase in capelin abundance resulted from a movement of capelin into the area or from a resurgence of a small local population under favorable conditions. On Flemish Cap, capelin had not appeared as bycatch in groundfish surveys between 1949 and 1985 or in predator stomachs examined between 1978 and Prior to their appearance in the 1990s, the only record was a bycatch in a commercial fishery in Both the 1973 record and the appearances in the 1990s coincided with below average water temperatures. Since capelin had not occurred as bycatch in most years, it is likely that the occurrences during cold years were the result of migration to the area when temperature conditions were favorable. It has not been possible to determine whether the appearance of capelin in these areas could account for the decline in the acoustic estimates; however, bycatch increases have been significant. In 1993, catch rates increased by a factor of 100 on Scotian Shelf and capelin occurred in 72% of the 1,103 observed shrimp fishing sets on Flemish Cap (total capelin bycatch weight = 4,811 kg). Spawning times and mean lengths Peak spawning time of capelin along the northeast coast of Newfoundland has been several weeks later since 1991 (Figure 4) and this shift has been statistically linked with colder water temperatures during the maturation period just prior to spawning (Carscadden et al. In press). During the 1990s, the population mean lengths of mature capelin were smaller than mature capelin during the 1980s (Figure 4). The population mean length was smaller because of smaller fish of age-3 and older and an increased contribution of age-2 fish to the spawning stock. Carscadden et al. (In press) have shown that the time of peak spawning is also related to mean size of fish in the population, with later spawning occurring when fish are smaller. When combined with prespawning water temperatures, mean length explained 80% of the variation in peak spawning. The occurrence of later-than-expected spawning influenced the timing of the aerial survey and disrupted the commercial fishery. During the 1980s, the aerial survey was arranged for a specific period, mid-june to early July. Even in 1985, when spawning was later and related to cooler water temperatures (Nakashima 1996, Carscadden et al. In press), the abundance peak was detected near the end of the survey period. Howev-

7 Forage Fishes in Marine Ecosystems 463 Figure 4. Peak spawning time (day of the year) of capelin, ( ), and mean lengths of capelin (mm) with 95% confidence intervals, ( ). er, the extremely late arrival of capelin inshore in 1991 was unexpected and the survey ended before the peak abundance of capelin occurred near the beaches (Nakashima 1996a). After the 1991 experience, more flexibility in timing was built into the aerial survey and peak spawning has been better covered. Nevertheless, the unpredictable nature of the peak spawning time has caused difficulties in planning the aerial survey since The trap catch rate data have also been more difficult to interpret because of the changing nature of the fishery due to changes in capelin biology and changes in management measures. During the 1980s, opening dates of the fishery were often well before the peak run of capelin and traps were fished as the capelin moved into the area and until the quota was reached. Furthermore, each fisherman was responsible for assessing the market suitability of his catch. However, during the 1990s, the fishing pattern changed when a catch monitoring program was initiated preventing the fishery from opening until fish met specific market criteria. Thus, the potential existed under this monitoring procedure for the fishery to open during the peak of the run, thereby affecting catch rate estimates. The fishery in the 1990s was further affected by fish size regulations in the management plan. Larger females were in greater demand but with fish sizes becoming smaller during the early 1990s, the

8 464 Carscadden & Nakashima Capelin Abundance in Cooler Waters potential for excessive discarding increased. In 1994 a size criterion was included in the management plan such that the fishery did not open until female capelin exceeded a critical size (<50 females/kg). This management initiative effectively prevented the fishery from opening during 1994 and 1995, so that there were no catch rate data for those years. The initiation of a monitoring program to determine the fishery opening coincident with a size regulation in the management plan and small average fish sizes has created a fishing situation different from that observed in the 1980s. If fish sizes increase and a fishery resumes with either monitoring or fish size regulations in effect, the catch rate data will have to be carefully evaluated. Interpretations of Abundance Indices The changes in biology of capelin during the early 1990s affected not only the collection and interpretation of data on individual indices but also the integration and evaluation of the suite of indices used in assessing stock status. The primary problem has been the reconciliation of the very low acoustic estimates in the 1990s and the relatively unchanged inshore abundance indices (Figure 5). Because the inshore indices did not decline to the extent predicted by the acoustic surveys, the suspicion was that the acoustic surveys were not accurately tracking trends in total abundance, although there were no reasons to reject the estimates on technical grounds. However, many of the assumptions underlying the inshore indices had never been tested and so inshore indices were also questioned to some extent, particularly since the changes in biology most apparent in the spawning stock (e.g., late arrival and smaller mean sizes) were complicating the collection of data for these indices. In an attempt to evaluate the different patterns between acoustic estimates and inshore indices, other sources of data were examined. We have already outlined the evidence for changes in distribution within the usual range of capelin in Div. 2J3K as well as the increase in abundance on Scotian Shelf and Flemish Cap. Special studies on densities of eggs and larvae on several Newfoundland beaches beginning in 1991 confirmed the existence of capelin spawning throughout the 1990s, contrary to a public perception that capelin had not spawned at all. Unfortunately, no egg density estimates for comparable beaches were available for the 1980s and as a result, it was not possible to determine from the egg deposition alone whether a decline in spawning stock abundance had occurred. However, observations made during the late 1980s from beaches in a small portion of the larger geographic sampling area suggested that capelin egg deposition had not declined to the extent predicted from the acoustic surveys (Nakashima and Slaney 1994). Besides the distributional changes demonstrated by the groundfish surveys, the results from the surveys were also examined to determine

9 Forage Fishes in Marine Ecosystems 465 Figure 5. Relative trends in acoustic abundance estimates. Each index is standardized to the highest value within that series. Acoustic estimates ( ) are for Division 3L, spring and fall , from Miller (1992, 1993, 1994); aerial estimates ( ) are from Nakashima (1996b); and catch rates ( ) are for trap nets from Nakashima (1994). whether they could be used as abundance indicators. Frequency of occurrence was thought to describe general abundance trends on the assumption that for pelagic species the range of a species may be a direct function of stock biomass levels (Anon. 1995). Although this assumption has not been tested in this particular application, the trends in frequency of occurrence have not shown dramatic declines during the 1990s. Finally, there was growing evidence from bycatches of age-0 (Anderson and Dalley 1996) and age-1 capelin (Dalley et al. 1996) in young fish surveys designed for gadoids, that these younger age groups were abundant and widely dispersed offshore throughout Div. 3K and Div. 3L. Like the beach surveys for eggs, these surveys were initiated only in the 1990s, during the period of anomalous hydrographic conditions, and therefore comparisons with a more normal period could not be made. However, as more surveys were completed and young capelin appeared abundant and widespread, these results seemed to support the optimistic inshore indices of abundance rather than the pessimistic offshore acoustic results.

10 466 Carscadden & Nakashima Capelin Abundance in Cooler Waters Discussion It is clear that there were significant variations in the biology and behavior of capelin during the first half of the 1990s, as evidenced by the distribution anomalies over wide geographic areas, decrease in sizes of mature individuals, and delays in peak spawning times by up to 1 month. These changes coincided with below average water temperatures which persisted over a large part of the northwest Atlantic. In addition, abundance indices for capelin exhibited divergent trends. The dichotomy in patterns of abundance indices, offshore and inshore, has never been fully reconciled. However, based on available evidence to date, it now appears that the acoustic surveys were underestimating the true population abundance of capelin offshore. The occurrence of capelin in areas where they do not usually occur, especially Flemish Cap, the continued occurrence of capelin as bycatch in groundfish surveys, the widespread distribution of young capelin in age-0 and juvenile surveys throughout the area, and the continued spawning of capelin on beaches inshore suggest that capelin abundance did not decline to the extent predicted by the acoustic surveys. Recent evidence (Miller 1996) from special acoustic experiments suggests that capelin may have been undetectable by the acoustic gear because they were scattered rather than in schools. It seems likely that the severe environmental conditions during the early 1990s were the major cause of the changes in biology and behavior of capelin, and these changes had their greatest impact on the acoustic estimates. Acknowledgments We acknowledge the work of many individuals in the Department of Fisheries and Oceans, St. John s, who collected and analyzed data on capelin, groundfish, and oceanography over many years. We are especially grateful for the assistance of M. Rees, D.S. Miller, J. Simon, K. Frank, and E. Colbourne in the final preparation of the manuscript. References Anderson, J.T., and E.L. Dalley Distribution and abundance of pre-recruit capelin (Mallotus villosus) in the Newfoundland Region (2J3KL), 1994 and In: Anon., Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 96/90, 269 pp. Anon Capelin in SA2 + Div. 3KL. DFO Atl. Fish. Res. Doc. 95/70, 338 pp. Bakanev, V.S Results from acoustic capelin surveys in Div. 3LNO and 2J + 3KL in NAFO SCR Doc. 92/1, Ser. No. N2034, 12 pp. Carscadden, J.E Bycatch of capelin in shrimp fisheries in NAFO Div. 2J3K and Div. 3M. In: Anon., Capelin in SA2 + Div. 3KL. DFO Atl. Fish. Res. Doc. 96/90, 269 pp.

11 Forage Fishes in Marine Ecosystems 467 Carscadden, J., B.S. Nakashima, and K.T. Frank. In press. The effects of fish length and temperature on the timing of peak spawning in capelin (Mallotus villosus). Can. J. Fish. Aquat. Sci. Carscadden, J., B. Nakashima, and D.S. Miller An evaluation of trends in abundance of capelin (Mallotus villosus) from acoustics, aerial surveys and catch rates in NAFO Division 3L, J. Northw. Atl. Fish. Sci. 17: Dalley, E.L., J.T. Anderson, and J.E. Carscadden Capelin bycatches from demersal juvenile cod surveys, In: Anon., Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 96/90, 269 pp. Drinkwater, K.F Atmospheric and oceanic variability in the northwest Atlantic during the 1980s and early 1990s. J. Northw. Atl. Fish. Sci. 18: Frank, K.T., J.E. Carscadden, and J.E. Simon Recent excursions of capelin (Mallotus villosus) to the Scotian Shelf and Flemish Cap during anomalous hydrographic conditions. Can. J. Fish. Aquat. Sci. 53: Lilly, G.R By-catches of capelin in bottom-trawl surveys. In: J. Carscadden (compiler), Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 94/18, 164 pp. Lilly, G.R By-catches of capelin during autumn bottom trawl surveys in Divisions 2J3KLNO, with emphasis in In: Anon., Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 95/70, 338 pp. Lilly, G.R., and D.J. Davis Changes in the distribution of capelin in Divisions 2J, 3K and 3L in the autumns of recent years, as inferred from bottomtrawl by-catches and cod stomach examinations. NAFO SCR Doc. 93/54, Ser. No. N2237, 14 pp. Miller, D.S An estimate of capelin (Mallotus villosus) biomass from an acoustic survey conducted in NAFO Divisions 2J3K in October, CAFSAC Res. Doc. 90/8, 18 pp. Miller, D.S Results of an acoustic survey for capelin (Mallotus villosus) in NAFO Division 3L in NAFO SCR Doc. 92/57, Ser. No. N2110, 4 pp. Miller, D.S Observations and studies on SA2 + Div. 3K capelin in CAFSAC Res. Doc. 93/10, 10 pp. Miller, D.S Results from an acoustic survey for capelin (Mallotus villosus) in NAFO Divisions 2J3KL in the autumn of In: J. Carscadden (compiler), Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 94/18, 164 pp. Miller, D.S Observations on the relationship between acoustic estimates and trawl catches. In: Anon., Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 96/90, 269 pp. Nakashima, B.S The inshore capelin fishery in NAFO Div. 3Kl in In: J. Carscadden (compiler), Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 94/18, 164 pp. Nakashima, B.S. 1996a. The relationship between oceanographic conditions in the 1990s and changes in spawning behaviour, growth and early life history of capelin (Mallotus villosus). NAFO Sci. Coun. Stud. 24:55-68.

12 468 Carscadden & Nakashima Capelin Abundance in Cooler Waters Nakashima, B.S. 1996b. Results of the 1995 CASI aerial survey of capelin (Mallotus villosus) schools. In: Anon., Capelin in SA2 + Div. 3KL. DFO Atl. Fish. Res. Doc. 96/90, 269 pp. Nakashima, B.S., and B. Slaney Capelin (Mallotus villosus) egg deposition on fifteen spawning beaches in Conception Bay, Newfoundland in In: J. Carscadden (compiler), Capelin in SA2 + Div. 3KL, pp DFO Atl. Fish. Res. Doc. 94/18, 164 pp.

13 Proceedings Forage Fishes in Marine Ecosystems 469 Alaska Sea Grant College Program AK-SG-97-01, 1997 The Barents Sea Capelin Stock (Mallotus villosus): A Brief Review Harald Gjøsæter Institute of Marine Research, Bergen, Norway Abstract The stock of capelin inhabiting the Barents Sea is potentially one of the largest capelin stocks in the world, with a historical biomass of 6-10 million tons. It serves as a forage fish for various predators in the area, including fish (mainly cod), sea mammals, and birds. Stock size has been monitored since 1972 by means of acoustic methods, and biological sampling has been quite intensive. In and in , the stock collapsed. These events have been explained as a combined effect of recruitment failure due to predation from herring on capelin larvae, increased natural mortality due to predation from cod on adult capelin, over-exploitation, and reduced growth due to environmental changes. This paper presents the time series of acoustic stock size estimates for the period , and describes various aspects of the history of this stock since The capelin s role as a forage fish in the Barents Sea ecosystem is discussed, and some estimates of the amount of capelin consumed by its predators are presented. Background The area The Barents Sea is a high-latitude, shallow continental shelf area. It is bounded in the north by the archipelagos of Spitsbergen and Franz Josef Land, in the east by Novaya Zemlya, and in the south by the coasts of northern Norway and Russia (Figure 1). In the west, the boundary between the Barents Sea and the Norwegian Sea is usually drawn along the continental edge at about East Longitude. More than 20% of the area is shallower than 100 m, but troughs deeper than 400 m enter the area from the west and northeast.

14 470 Gjøsæter Review of the Barents Sea Capelin Stock Figure 1. Map of the Barents Sea showing a generalized distribution area for capelin. Climatic features Temperature, ice, and current conditions are considered to be important for the biological production processes that take place in the Barents Sea (Loeng 1991). Helland-Hansen and Nansen (1909), studying the oceanographic conditions of the Barents Sea, stated that it is to be expected that variations in the physical conditions of the sea have a great influence upon the biological conditions of various species of fishes living in the sea, and it might therefore also be expected that such variations are the primary cause of the great and hitherto unaccountable fluctuations in the fisheries. Since then, several studies have strengthened this view. Currents and water masses in the Barents Sea The Norwegian Coastal Current flows along the coast of Norway and Russia, given the name Murman Coastal Current when it crosses the border between the two countries. The Norwegian Atlantic Current flows into the Barents Sea from the southwest, dividing into two branches flowing east and northeast. Arctic water enters the Barents Sea through the channel between Spitsbergen and Franz Josef Land and, more important, between Franz Josef Land and Novaya Zemlya (Loeng 1991).

15 Forage Fishes in Marine Ecosystems 471 The three main water masses of the Barents Sea Coastal Water, Atlantic Water, and Arctic Water are linked to these current systems. In addition, locally formed water masses resulting from processes taking place inside the area, e.g., seasonal freezing and melting of ice, can be found. Where the Atlantic and Arctic water meet, a well-defined polar front is formed. Its position is rather stable in the area south of Spitsbergen, where it is governed by the bottom topography, but is more variable in the eastern parts of the Barents Sea. Climatic variability Several authors have suggested that the variability of oceanographic features in the Barents Sea is of advective nature, closely related to meteorological conditions (Loeng et al. 1991). Long time series of temperature in various hydrographic sections are available, of which the longest series is from the Kola section observed by Russian scientists at monthly or quarterly intervals from Mathematical analyses of the observations from this and other sections have revealed cyclic events with periodicity from about 3 years to years (Loeng et al. 1991). Ådlandsvik and Loeng (1991) found a very close relationship between calculated inflow of Atlantic water and the temperature anomalies inside the Barents Sea. They suggested that the climate of the Barents Sea oscillates between two states: warm and cold. The warm state is characterized by high temperatures, low air pressure, cyclonic circulation in the atmosphere, increased Atlantic inflow, and little ice coverage. The cold state is characterized by low temperatures, high air pressure, anticyclonic air circulation, decreased Atlantic inflow, and more severe ice conditions. Positive feedback mechanisms maintain the system in one of the states, while a transition from one state to the other is likely to be enforced by larger-scale oceanic and atmospheric circulation. The climate has been shown to affect the fish populations in the Barents Sea in various ways. Sætersdal and Loeng (1987) demonstrated that good recruitment in the stocks of cod, haddock, and herring was associated with increased inflow of Atlantic water to the Barents Sea. Increased environmental temperature has been found to promote the growth of cod (Nakken and Raknes 1987) and capelin (Gjøsæter and Loeng 1987). The distribution of cod and haddock (Shevelev et al. 1987) and capelin (Ozhigin and Ushakov 1985, Gjøsæter and Loeng 1987) is affected by the heat content of the water masses. The large temperature fluctuations that have occurred since the mid-1970s have had a great effect both on the spawning and feeding migrations and on the distribution of spawning, feeding, and overwintering of capelin (Gjøsæter 1995). The capelin stock The capelin is a small, schooling, pelagic, salmonid fish inhabiting subarctic and arctic regions. One large oceanic stock is found in the Barents Sea, potentially one of the largest capelin stocks in the world. During

16 472 Gjøsæter Review of the Barents Sea Capelin Stock summer and autumn the adult stock is found in the central to northern part of the Barents Sea, feeding heavily on copepods and euphausiids. During late autumn the stock concentrates in an area south of the polar front, and during January-March the maturing part of the stock (3-5 years old, larger than about 14 cm) starts a migration toward the spawning grounds near the coasts of northern Norway and Russia. Spawning takes place in March-April, and the demersal eggs are laid on sand and gravel spawning beds at depths of m. Spawning mortality is substantial, and in addition there is normally a very high predation risk due to young cod gathering at the coast to feed on capelin during spring. Consequently, few individuals survive to spawn a second time (Gjøsæter 1995). The eggs hatch after 3-6 weeks, depending on temperature (Gjøsæter and Gjøsæter 1986), and the larvae spread out into the southern parts of the Barents Sea. In the autumn, the young-of-the-year capelin normally show a widespread distribution in the areas south of 76 N. The young (immature and maturing) capelin take up a seasonal migrating pattern. From the wintering areas they often move towards the coast in early summer to graze the spring bloom there, but then migrate north and east during summer, following the receding ice edge and the plankton bloom associated with it (Hassel et al. 1991, Skjoldal et al. 1992). Other important stocks in the area Other fish stocks Relatively few fish species are found in the Barents Sea, but some species found there are very numerous. Apart from capelin, Atlantic cod (Gadus morhua), Atlantic herring (Clupea harengus) and Arctic cod (Boreogadus saida) form important parts of the ecosystem. Cod and herring spawn outside the area, but cod live there most of their lives and herring use the Barents Sea as a nursery area; the young stay there from their first to their third or fourth year of life. Cod are predatory fish which, apart from the youngest stages, primarily eat fish (Mehl 1991, Bogstad and Mehl 1997). The size of the cod stock varied between 1 million and 3 million tons in the period The herring also plays an important role in the Barents Sea, although it is not always present there, and the year classes spend a maximum of 4 years there. The recruitment to the stock of Norwegian spring spawning herring is extremely variable; very numerous year classes emerge at about 10-year intervals, and the recruitment in the intervening periods is variable but mostly poor (Hamre 1988). When the larval survival of herring is good, most of the larvae are transported into the Barents Sea and stay in the southern parts of the area until they reach about 25 cm in length at age 3 or 4. In years of poor herring recruitment practically no herring larvae enter the Barents Sea.

17 Forage Fishes in Marine Ecosystems 473 The Arctic cod is a semipelagic species inhabiting the eastern and northern parts of the Barents Sea. Like capelin, Arctic cod spend their whole life in the Barents Sea. This species is a forage fish serving as food for other fish, seals, whales, and birds. The stock history of Arctic cod in the Barents Sea is presented and discussed by Gjøsæter and Ushakov (1997) in another paper presented at this symposium. Seals The most important seals in the Barents Sea are the ringed seal (Phoca hispida) and the harp seal (P. groenlandica). The ringed seal is found near ice throughout the year, while the harp seal leads a pelagic life apart from the breeding and molting season, when it is found on the White Sea ice. Both species prey on fish: the ringed seal primarily on Arctic cod, and the harp seal on herring, capelin, Arctic cod, and others. Whales Of the baleen whales, the blue (Balaenoptera musculus), minke (B. acutorostrata), fin (B. physalus), and humpback (Megaptera novaeangliae) whales migrate into the Barents Sea during summer, and small numbers of bowhead whales (Balaena mysticetus) occur around Franz Josef Land. Of the toothed whales, the white whale (Delphinapterus leucas) and the narwhal (Monodon monoceros) are relatively common in ice-covered waters, while the killer whale (Orcinus orca), white-beaked dolphin (Lagenorhynchus albirostris), and harbor porpoise (Phocoena phocoena) mainly occur in the southern, ice-free parts of the region (Hansen et al. 1996). Only the minke whale is found in large quantities in the Barents Sea (Sakshaug et al. 1992). The toothed whales mostly eat fish and squid. The baleen whales feed on both zooplankton and fish, and the diet of the minke whale consists primarily of various fish species (Haug et al. 1995a,b). Birds More than 30 species of seabirds have been recorded in the Barents Sea region, but only a few of these constitute the majority of the biomass and are important in the overall ecology of the marine ecosystem (Hansen et al. 1996). The main species are northern fulmar (Fulmarus glacialis), glaucous gull (Larus hyperboreus), black-legged kittiwake (Rissa tridactyla), common murre (Uria aalge), Brünnich s guillemot (U. lomvia), black guillemot (Cepphus grylle), razorbill (Alca torda), Atlantic puffin (Fratercula arctica), dovekie (Alle alle,) and common eider (Somateria mollissima). The main fish feeders are the alcids, of which the common murre and Atlantic puffin have specialized on the pelagic schooling species herring and capelin, while Brünnich s guillemot takes some zooplankton organisms in addition to capelin and Arctic cod (Sakshaug et al. 1992).

18 474 Gjøsæter Review of the Barents Sea Capelin Stock Materials and Methods The primary material for this paper is a time series of acoustic estimates of stock size of capelin (see below). Parts of this time series have been published before (Dommasnes and Røttingen 1985, Gjøsæter 1995), data from 1995 are from the International Council for the Exploration of the Sea (ICES 1996), and data from 1996 from an unpublished survey report. This time series is used both to represent the stock size and to estimate mortality and stock production. In combination with fishery statistics, the mortality estimates are also partitioned on fishing mortality and natural mortality. Another data source utilized is a time series of estimates of cod s consumption of capelin from 1984 to 1995 (Bogstad and Mehl 1997). Estimates of consumption of capelin by seals, whales, and birds are from the literature. Capelin surveys Since 1972, the Barents Sea capelin stock has been monitored during annual Norwegian-Russian acoustic surveys (Nakken and Dommasnes 1975, 1977; Dommasnes and Røttingen 1985) mostly applying standard methods (MacLennan and Simmonds 1992). The acoustic equipment has changed over the years, but the echosounders have been calibrated according to standard procedures (Foote et al. 1983), and during the autumn surveys the vessels are in addition compared when covering parts of a transect together. The time series of acoustic estimates of capelin from these surveys should, therefore, be consistent. Acoustic stock size estimation procedure The basic relationship between the echo density, or area backscattering coefficient s A (the output from the echo integrators), and the area density (number of fish per unit area) r A is s A = s r A (1) where the proportionality factor s is called the mean acoustic cross section (MacLennan and Simmonds 1992) and is a measure of the fish s ability to reflect sound. When the mean echo density in a unit area and the sound reflection characteristics of the insonified fish targets are known, the number of fish (N) can be found: N A s A = r A = A (2) s If the mean weight ( w ) of these fishes is known, the biomass (B) can be found: B = N w (3) The acoustic cross section of a fish (the logarithmic form is called target strength, TS) is length dependent. The relationship between target

19 Forage Fishes in Marine Ecosystems 475 strength and fish length is empirically established for each species. When the acoustic method was introduced for capelin in the early 1970s, no target strength measurements were available for this species. A conversion factor between integrator output and number of fish was established by counting fish traces on the echograms (Midttun and Nakken 1971). This gave rise to varying conversion factors during the early 1970s (Dommasnes and Røttingen 1985). A part of this variation was probably due to variations in the performance of the acoustic systems. Gradually, estimates of capelin target strength and its dependency on length became available (Dommasnes and Røttingen 1985), and estimates obtained in previous years were recalculated accordingly. Since 1985, a TS-length relation of TS = 19.1 log L 74.0 has been used for capelin in the Barents Sea, corresponding to s = L All estimates presented in this paper are based on this target strength value. The results from the autumn surveys are not presented directly, for two reasons. First, in some years catches were taken prior to or during the survey period in September and October, and all survey results were therefore back calculated to a date before opening of the autumn fishing season (August 1), taking account of fishing and natural mortality. Second, prior to 1980, the southeastern Barents Sea, where some of the 1-group capelin are normally found during autumn, was not properly covered during the acoustic surveys, and the 1-group estimates for the years prior to 1980 were estimated from the 2-group estimate the preceding year, taking account of fishing and natural mortality (ICES 1996). In 2 years after 1980 (1989 and 1993) the 1-group acoustic estimates were lower or equal to the corresponding 2-group estimates the year after. In these cases, I chose to keep the 2-group estimates, and adjust the 1-group estimates so that the reduction in number between age 1 and age 2 was equal to the mean of those measured the year before and the year after. Capelin stock production The biomass produced in the capelin stock per year is partly lost or output to the ecosystem, partly harvested by man, and partly added to the standing stock. The part output through natural mortality (called M output biomass by Hamre and Tjelmeland 1982) has been estimated by calculating the reduction in number during 1 year multiplied by the mean weight of these individuals. In practice this is done separately for each age group in the stock, for the immature and mature component of each age group, and for two separate seasons. Results and Discussion Stock history of capelin The stock size changed dramatically during the period (Figure 2). Maximum stock biomass was observed in 1975 at above 6 million

20 476 Gjøsæter Review of the Barents Sea Capelin Stock metric tons, but stock size was also very large in 1980 and Two stock collapses occurred in the period: from 1983 to 1986, and then again from 1992 to 1994, the stock decreased from an average size of 3-5 million tons to below 200,000 tons. The dramatic decrease seen in these two periods is contrasted by an even more dramatic increase in stock size from 1989 to Gjøsæter (1995) argued that this stock history can be explained from what is known about the population dynamics of this species and the ecological conditions in the area. Although the stock was heavily exploited from the mid-1970s up to the first stock collapse, fishing played a minor role in the first collapse and practically no role at all in the second (Figure 3). The key to the changes in stock size is partly found in the life history of the capelin (characterized by a very flexible, density-dependent growth rate, length-dependent maturation, and almost total spawning mortality), and partly in the biotic and abiotic environmental factors in the area (periodic changes in sea climate and in size and geographical distribution of the stocks of predators in the Barents Sea). The period was characterized by a declining cod stock and no herring in the Barents Sea (Figure 4). The capelin stock was large (>4 million tons) and was heavily exploited (the landings varied from 1.2 million to 3.0 million tons). The increase in the capelin stock size from 1972 to 1975 has been explained by recruitment of the three large but slow-growing year classes (Gjøsæter 1995). Since slow growth implies late maturation, and therefore delayed spawning mortality, the stock grew by accumulation of immature fish (Figure 2). The sudden fall in stock size from 1975 to 1977 was likewise explained by the bulk of this accumulated stock spawning (and dying) without new strong year classes to replace it. The peak in stock biomass in 1980 was caused by a substantial rise in individual growth while the stock consisted of year classes of intermediate sizes. The number of individuals in the stock was lower in 1980 than in 1978, while the biomass was much higher (Figure 2). The increased growth made a high proportion of capelin to spawn in the following year, and the stock size was once more somewhat reduced. The stock collapsed following a recruitment failure in 1984 and the following years (Figure 2). Simultaneously, the mortality caused by predation rose dramatically when an increasing cod stock fed on a reduced capelin stock (Figure 3), and the individual growth was reduced (Skjoldal et al. 1992). The fishery on the capelin in the and fishing seasons added to the other factors, and consequently the capelin stock was reduced to a very small size in 1986 (Figure 3). The capelin stock regained its pre-collapse size very rapidly because of a very numerous year class in 1989 and record individual growth in 1990, only to dwindle once more in The mechanisms involved in this second collapse were the same as those in the first, but the fishery was insignificant (Figure 3) and individual growth was

21 Forage Fishes in Marine Ecosystems 477 Figure 2. Barents Sea capelin stock history, Columns denote number of fish in age groups (left axis), solid line is the total number in age groups 1-5 (left axis), and dotted line is the total stock biomass (right axis). Figure 3. Capelin M output biomass (see text for explanation), capelin catch, and capelin consumed by cod, whales, seals, and birds.

22 478 Gjøsæter Review of the Barents Sea Capelin Stock Figure 4. Stock history (biomass) of capelin, cod, and herring in the Barents Sea after relatively stable. As seen from Figure 4, the recruitment failure of capelin in 1984 and 1985, and in , occurred when Norwegian spring spawning herring were abundant in the Barents Sea. This occurs sporadically, and has an adverse effect on capelin recruitment because the young herring feed on capelin larvae (Huse and Toresen 1995). In 1996, the amount of herring in the Barents Sea was once more heavily reduced (Figure 4), and the first signs of the capelin stock recovering from the collapsed state occurred (Figure 2), first of all as an increased number of 1-year-old capelin. In 1996, a relatively high number of capelin larvae was detected during a cruise in June-July (Unpubl. data, Institute of Marine Research, Bergen). The highest concentration of herring and the highest concentration of capelin larvae overlapped in June-July, which may indicate that predation from herring on capelin larvae can be substantial. The role of capelin as a forage fish The capelin is one of the primary forage fishes in the Barents Sea, serving as food for predatory fish (Bogstad and Mehl 1997), whales (Haug et al. 1995a,b; Nordøy et al. 1995a), seals (Nordøy et al. 1995b), and birds (Sakshaug et al. 1992, Hansen et al. 1996). In addition, capelin have been heavily exploited by the fisheries (Gjøsæter 1995). This species plays a key role in the Barents Sea ecosystem, harvesting the rich plankton production in the northern areas and making this production avail-

23 Forage Fishes in Marine Ecosystems 479 able both to predators inhabiting these areas and to those restricted to the more southern areas of the Barents Sea (Hamre 1994). Obtaining quantitative information on the capelin s role as a forage fish is difficult, for several reasons. First, such estimates are based either on stomach content analyses of field-sampled animals or calculations of energy requirements based on captive animals offered various kinds of food. Both methods are based on assumptions which may or may not be realistic when extrapolating in time and space. Second, going from individual modeled food requirements or modeled food intake per day to a whole stock of such individuals food intake per month or year may give unrealistic results, because consumption will certainly be dependent on overlap in time and space of predator and prey stocks, availability of prey (prey stock size and behavior), availability of alternative prey, environmental conditions (e.g., temperature which affects digestion rates), and other factors. Finally, the consumption estimates will rely on a realistic predator stock size estimate, which is not always easy to obtain. Consequently, all estimates of consumption should be regarded as uncertain. In spite of this, such estimates may give clues to the relative importance of predators and prey, and the importance of predation among various causes of natural mortality in a species. Various consumption estimates have been obtained for the main predators on capelin. Bogstad and Mehl (1997) reported a time series of annual consumption estimates back to 1984 (Figure 3), which show that cod is a very important predator on capelin, and may in some years remove a considerable amount of the total production of capelin. In Figure 3 are also given the M output biomass and the catches of capelin. It is seen that in some years estimated consumption by cod was as high as or even higher than total capelin biomass output by natural mortality. Either the consumption estimates are too high or the output biomass estimates are too low, or both. Each curve shows the same trend, and the estimates can be reconciled using a scaling factor. The catches of capelin are in all years after 1984 considerably lower than the amount consumed by cod, and also lower than the total estimated M output biomass. For whales, seals, and birds no time series of consumption estimates are available. However, various point estimates have been reported. For the minke whale, the most important capelin predator among the whales, Nordøy et al. (1995a) estimated that during an assumed average stay of 6 months in the northeastern Atlantic the stock consumed 1.4 million tons of various prey. This estimate was based on energy requirements of growing and adult animals, on estimates of the composition of the diet from 1992, and an estimated stock size of 87,000 animals. The calculations suggest that the northeastern Atlantic minke whale population consumes about 355,000 tons of capelin (Figure 3). Since the calculations were based on diet composition for the Barents Sea (Haug et al. 1995a), and a part of the northeastern Atlantic whale

24 480 Gjøsæter Review of the Barents Sea Capelin Stock stock does not enter this area, this might be an overestimate. On the other hand, the latest revision of the stock size estimate of this whale population, based on sighting surveys carried out in 1995, is considerably higher: 112,000 animals (International Whaling Commission 1996). An estimate of the Barents Sea harp seal stock s consumption of capelin is also available (Nordøy et al. 1995b), based on observed daily food intake of captive harp seals and on analysis of stomach contents in Nordøy et al. (1995b) arrived at an estimate of annual food consumption of this population of 1 million tons. Of this, about 700,000 tons consisted of various fish species, of which capelin (250,000 tons) and herring (200,000 tons) were the most important (Figure 3). These calculations are based on a harp seal population of 600,000 animals. The researchers argued that the results may be biased toward underestimating the proportion of fish in the diet. Most of the stomach material was collected from seals caught in the pack ice, and consequently the amphipod Themisto libellula, particularly abundant in close vicinity to pack ice, may be over-represented. Mehlum and Gabrielsen (1995) estimated the food requirement of the total population of seabirds at 5,600 tons per day during the 250- day period they stayed in the Barents Sea, amounting to about 1.4 million tons of food annually from the Barents Sea. An estimate of the proportion of capelin from this total food base is not available. The common murre represents about 10% of the total food requirement, and this species mostly eats capelin. Brünnich s guillemot represents 55%, but has a much lower proportion of capelin in its diet. A total mean capelin consumption of about 200, ,000 tons could be a fair guess, and a value of 250,000 tons is indicated for the year 1991 in Figure 3. Summing up, capelin obviously play a key role as forage fish in the Barents Sea marine ecosystem. While playing this role, the Barents Sea capelin stock itself undergoes large fluctuations, partly because of changing environmental forces, partly as a feedback from other species in the ecosystem. The estimates of capelin consumption by whales, seals, and birds are indicated in Figure 3 for the relevant years. Compared to consumption by cod, consumption by these predators seemingly plays a minor role. There is strong evidence that other species higher up in the food web have been affected by the changes in capelin stock size. The individual growth of cod was seriously reduced during the capelin stock collapse in (Mehl 1991). After the capelin stock had collapsed in 1986, about 1 million common murres died during the winter of On Bear Island, where most of the common murres in the Barents Sea breed, 85-95% of the breeding population disappeared in the course of 1 year. A similar situation was observed along the Finnmark coast of northern Norway (Sakshaug et al. 1992). Harp seals in some years invade the coast and fjords of Finnmark, apparently because of lack of

25 Forage Fishes in Marine Ecosystems 481 food in offshore areas. The latest large seal invasion to this area was in 1987, when a considerable number of seals died from starvation or drowned in fishing nets along the coast of northern Norway. The whale stocks are probably less dependent on capelin as food, but may change feeding migrations during periods when the capelin stock is low. During the sighting surveys for minke whales in 1995, a considerably smaller part of the whale stock was detected in the Barents Sea than was the case during previous years of such surveys (Pers. comm., Nils Øien, Institute of Marine Research, Bergen, July 1996). This could be a reaction to the low abundance of capelin in the Barents Sea in Therefore, even though predation from whales, seals, and birds may play a minor role for the capelin stock in periods when capelin are found in normal quantities, the presence of capelin is vital for at least some of these stocks, and the lack of capelin during periods of stock collapses may have a serious effect on these. References Ådlandsvik, B., and H. Loeng A study of the climatic system in the Barents Sea. In: E. Sakshaug, C.C.E. Hopkins, and N.A. Øritsland (eds.), Proceedings of the Pro Mare Symposium on Polar Marine Ecology, Trondheim, May Polar Res. 10(1): Bogstad, B., and S. Mehl Interactions between Atlantic cod (Gadus morhua) and its prey species in the Barents Sea. In: Forage Fishes in Marine Ecosystems. Alaska Sea Grant Report 97-01, University of Alaska Fairbanks, Fairbanks, AK (this volume). Dommasnes, A., and I. Røttingen Acoustic stock measurements of the Barents Sea capelin A review. In: H. Gjøsæter (ed.), Proceedings of the Soviet-Norwegian Symposium on the Barents Sea Capelin, Bergen, August Institute of Marine Research, Bergen, Norway, pp Foote, K., H.P. Knudsen, and G. Vestnes Standard calibration of echo sounders and integrators with optimal copper spheres. Fiskeridir. Skr. Ser. Havunders. 17: Gjøsæter, H Pelagic fish and the ecological impact of the modern fishing industry in the Barents Sea. Arctic 48(3): Gjøsæter, H., and J. Gjøsæter Observations on the embryonic development of capelin (Mallotus villosus Müller) from the Barents Sea. Fiskeridir. Skr. Ser. Havunders. 18: Gjøsæter, H., and H. Loeng Growth of the Barents Sea capelin, Mallotus villosus, in relation to climate. Environ. Biol. Fishes 20(4): Gjøsæter, H., and N.G. Ushakov Acoustic estimates of Barents Sea arctic cod stock (Boreogadus saida). In: Forage Fishes in Marine Ecosystems. Alaska Sea Grant Report University of Alaska Fairbanks, Fairbanks, AK (this volume).

26 482 Gjøsæter Review of the Barents Sea Capelin Stock Hamre, J Some aspects of the interrelation between the herring in the Norwegian Sea and the stocks of capelin and cod in the Barents Sea. ICES C.M. 1988/H: pp. Hamre, J Biodiversity and exploitation of the main fish stocks in the Norwegian/Barents Sea ecosystem. Biodiversity and Conservation 3: Hamre, J., and S. Tjelmeland Sustainable yield estimates of the Barents Sea capelin stock. ICES C.M. 1982/H: pp. Hansen, J.R., R. Hansson, and S. Norris (eds.) The state of the European arctic environment. EEA Environment Monograph 3. European Environment Agency, Copenhagen. 136 pp. Hassel, A., H.R. Skjoldal, H. Gjøsæter, H. Loeng, and L. Omli Impact of grazing from capelin (Mallotus villosus) on zooplankton: A case study in the northern Barents Sea in August In: E. Sakshaug, C.C.E. Hopkins, and N.A. Øritsland (eds.), Proceedings of the Pro Mare Symposium on Polar Marine Ecology, Trondheim, May Polar Res. 10(1): Haug, T., H. Gjøsæter, U. Lindstrøm, and K.T. Nilssen. 1995a. Diet and food availability for north-east Atlantic minke whales (Balaenoptera acutorostrata), during summer of ICES J. Mar. Sci. 52: Haug, T., H. Gjøsæter, U. Lindstrøm, K.T. Nilssen, and I. Røttingen. 1995b. Spatial and temporal variations in northeast Atlantic minke whale Balaenoptera acutorostrata feeding habits. In: A.S. Blix, L. Walløe, and Ø. Ulltang (eds.), Whales, seals, fish and man. Developments in Marine Biology 4. Elsevier, Amsterdam, pp Helland-Hansen, B., and F. Nansen The Norwegian Sea. Fiskeridir. Skr. Ser. Havunders. 2(2): Huse, G., and R. Toresen Predation by juvenile herring (Clupea harengus L.) on Barents Sea capelin (Mallotus villosus Müller) larvae. In: A. Hylen (ed.), Precision and relevance of pre-recruit studies for fishery management related to fish stocks in the Barents Sea and adjacent waters. Proceedings of the Sixth IMR-PINRO Symposium, Bergen, June Institute of Marine Research, Bergen, Norway, pp International Council for the Exploration of the Sea Report of the Northern Pelagic and Blue Whiting Fisheries Working Group. ICES C.M. 1996/Assess: pp. International Whaling Commission Report of the scientific committee Loeng, H Features of the physical oceanographic conditions of the Barents Sea. In: E. Sakshaug, C.C.E. Hopkins, and N.A. Øritsland (eds.), Proceedings of the Pro Mare Symposium on Polar Marine Ecology, Trondheim, May Polar Res. 10(1):5-18. Loeng, H., J. Blindheim, B. Ådlandsvik, and G. Ottersen Climatic variability in the Norwegian and Barents seas. ICES C.M. 1991/Variability Symposium pp.

27 Forage Fishes in Marine Ecosystems 483 MacLennan, D.N., and E.J. Simmonds Fisheries acoustics. Chapman and Hall, London. 325 pp. Mehl, S The northeast Arctic cod stock s place in the Barents Sea ecosystem in the 1980s: An overview. In: E. Sakshaug, C.C.E. Hopkins, and N.A. Øritsland (eds.), Proceedings of the Pro Mare Symposium on Polar Marine Ecology, Trondheim, May Polar Res. 10(1): Mehlum, F., and G.W. Gabrielsen Energy expenditure and food consumption by seabird populations in the Barents Sea region. In: H.R. Skjoldal, C. Hopkins, K.E. Erikstad, and H.P. Leinaas (eds.), Ecology of fjords and coastal waters. Elsevier, Amsterdam, pp Midttun, L., and O. Nakken Some results of abundance estimation studies with echo integrators. Rapp. P.-V. Reun. Cons. Int. Explor. Mer 170: Nakken, O., and A. Dommasnes The application of an echo integration system in investigations on the stock strength of the Barents Sea capelin (Mallotus villosus, Müller) ICES C.M. 1975/B: pp. Nakken, O., and A. Dommasnes Acoustic estimates of the Barents Sea capelin stock ICES C.M. 1977/H: pp. Nakken, O., and A. Raknes The distribution and growth of northeast Arctic cod in relation to bottom temperatures in the Barents Sea, Fish. Res. (Amst.) 5: Nordøy, E.S., L.P. Folkow, P.-E. Mårtensen, and A.S. Blix. 1995a. Food requirements of northeast Atlantic minke whales. In: A.S. Blix, L. Walløe, and Ø. Ulltang (eds.), Whales, seals, fish and man. Developments in Marine Biology 4. Elsevier, Amsterdam, pp Nordøy, E.S., P-.E. Mårtensson, A.R. Lager, L.P. Folkow, and A.S. Blix. 1995b. Food consumption of the northeast Atlantic stock of harp seals. In: A.S. Blix, L. Walløe, and Ø. Ulltang (eds.), Whales, seals, fish and man. Developments in Marine Biology 4. Elsevier, Amsterdam, pp Ozhigin. V.K. and N.G. Ushdov The effect of the thermal conditions of the sea and atmospheric circulation on the distribution of the Barents Sea capelin feeding areas. In: H. Gjøsæter (ed.) The proceedingsof the Soviet-Norwegian symposium on the Barents Sea Capelin. Institute of Marine Resarch, Bergen, Norway, pp Sætersdal, G., and H. Loeng Ecological adaptation of reproduction in northeast Arctic cod. Fish. Res. (Amst.) 5: Sakshaug, E., A. Bjørge, B. Gulliksen, H. Loeng, and F. Mehlum (eds.) The Barents Sea ecosystem. Pro Mare Norwegian Scientific Council, Norwegian Ministry of Environment. 304 pp. (In Norwegian.) Shevelev, M.S., V.V. Tereschenko, and N.A. Yaragina Distribution and behaviour of demersal fishes in the Barents and Norwegian seas, and the factors influencing them. In: H. Loeng (ed.), The effect of oceanographic conditions on distribution and population dynamics of commercial fish stocks in the Barents Sea. Proceedings of the Third Soviet-Norwegian Symposium, Murmansk, May 1986, pp

28 484 Gjøsæter Review of the Barents Sea Capelin Stock Skjoldal, H.R., H. Gjøsæter, and H. Loeng The Barents Sea ecosystem in the 1980s: Ocean climate, plankton, and capelin growth. ICES Mar. Sci. Symp. 195:

29 Proceedings Forage Fishes in Marine Ecosystems 485 Alaska Sea Grant College Program AK-SG-97-01, 1997 Acoustic Estimates of Barents Sea Arctic Cod Stock (Boreogadus saida) Harald Gjøsæter Institute of Marine Research, Bergen, Norway Nikolay G. Ushakov Polar Research Institute of Marine Fisheries and Oceanography, Murmansk, Russia Abstract The Barents Sea stock of Arctic cod (Boreogadus saida) (known there as Polar cod) is potentially one of the largest Arctic cod stocks in the world. It serves as a forage fish for predatory fish, sea mammals, and birds, and plays an important role in the ecosystem in the Arctic. In the late 1960s and early 1970s the stock was estimated at about 2 million metric tons and supported catches in the range of 200, ,000 metric tons. Since the mid-1970s the catches have been negligible. The stock size is poorly known for years prior to 1986, when routine acoustic stock size estimation was initiated on this species. This paper reviews the acoustic stock size estimates obtained for , and briefly describes various aspects of the recent history of this stock. Introduction The Arctic cod (Boreogadus saida Lepechin) is a circumpolar species, endemic to the arctic region. During most of the year, both adult and juvenile Arctic cod are found spread over the Barents Sea, excluding the southwestern parts most heavily affected by Atlantic water. Young-ofthe-year Arctic cod, on the other hand, are normally found in two separated areas during summer: in the eastern Barents Sea, and in an area near Spitsbergen (Figure 1). Consequently, there are seemingly two separate spawning areas: one in the southeastern area near Kolguev and Novaya Zemlya and one in the northwestern area near Spitsbergen (Gjøsæter 1973, Gjøsæter and Anthonypillai 1995). A western spawning area has, however, not yet been localized. It is also unknown whether

30 486 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Figure 1. Map showing the Barents Sea with the place names mentioned in the text. The hatched area is the general total distribution area of the Arctic cod stock (Boreogadus saida), while the spawning areas are crosshatched. two spawning areas implies that there are two separate stocks in the Barents Sea. Adult Arctic cod are present in the White Sea and in the Kara Sea, as well as in the areas north and northeast of the Barents Sea. It is unknown whether these Arctic cod are part of the Barents Sea stock, or belong to other (local) stocks. During the survey period in autumn, the Arctic cod has a wide distribution over the central and northern Barents Sea, feeding on the abundant plankton produced in these areas (Pechenik et al. 1973, Monstad and Gjøsæter 1987). Materials and Methods Since 1986, the Barents Sea Arctic cod stock has been monitored by acoustic methods and biological sampling during annual joint Norwegian-Russian trawl-acoustic surveys in autumn. The surveys, originally designed for capelin, from that year on have been aimed at complete coverage of all stocks of small pelagic fishes in the Barents Sea; i.e., capelin, Arctic cod, and herring. However, the capelin is still the most important target species, and when survey time is limited the coverage

31 Forage Fishes in Marine Ecosystems 487 of the Arctic cod stock suffers. Also, parts of the Arctic cod stock are found under ice and are inaccessible to acoustic surveying. The acoustic surveys are multiship surveys conducted by 3-5 scientific vessels from the Institute of Marine Research in Bergen and the Polar Research Institute of Marine Fisheries and Oceanography (PINRO) in Murmansk. They are conducted according to standard methods (MacLennan and Simmonds 1992), and the results are reported in survey reports prepared during meetings between Norwegian and Russian scientists upon completion of the surveys. Survey design The design of the annual Norwegian-Russian acoustic survey of the Barents Sea pelagic stocks is described in detail in, e.g., Nakken and Dommasnes (1975, 1977) and Dommasnes and Røttingen (1985). The initial survey area and the starting position are decided based on general knowledge of the fish distribution in the area, as well as observations made during the international 0-group trawl survey which is conducted immediately before the acoustic survey. The area is mostly covered by regularly spaced east-west transects, and each vessel covers every second transect. This design is adjusted near the border of the fish distribution area, where shorter tracks perpendicular to the border are made to ease the exact localization of the border. The degree of coverage (the distance between the tracks) is sometimes adjusted to the observed fish density, to secure a better coverage in areas of high density. Trawl hauls are taken regularly to monitor which species contribute to the recorded echo density along the tracks, and also to get samples of the target species to record length, weight, age, maturity, and other data. The echosounders are watched continuously, and trawling is conducted whenever the recordings change or there are other reasons to believe that the fish distribution has changed in any respect. The acoustic equipment has changed over the years. On the Norwegian vessels, the Simrad EK500 digital echosounder (Bodholt et al. 1989) and the BEI echo integrator and postprocessing system (Foote et al. 1991) were used from 1989, while on the Russian vessels this equipment was introduced in However, the echosounders have been calibrated according to standard procedures (Foote et al. 1987), and during the autumn surveys the vessels are in addition compared when covering parts of a transect together. The time series of acoustic estimates of Arctic cod from these surveys should, therefore, be consistent. Acoustic stock size estimation procedure The basic relationship between the echo density, or area backscattering coefficient s A (the output from the echo integrator) and the area density (number of fish per unit area) r A is s A = s r A (1)

32 488 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod where the proportionality factor is called the mean acoustic cross section (MacLennan and Simmonds 1992) and is a measure of the fish s ability to reflect sound. When the mean echo density in a unit area and the sound reflection characteristics of the insonified fish targets are known, the number of fish N in an area A can be found: N A s A = r A = A (2) s If the mean weight w of these fishes is known, the biomass B can be found: B = N w (3) The acoustic cross section of a fish (the logarithmic form is called target strength, TS) is length dependent. The relationship between target strength and fish length is empirically established for each species. When acoustic stock size estimation of Arctic cod was commenced in 1986, a target strength-length relation of TS = 21.8 logl 74.9 db, where L is fish length in centimeters, was applied to convert from echo abundance to fish density. This value was at that time used in abundance estimation of young gadoids (more or less of the same length as Arctic cod) in the North Sea. In 1988, a group of Russian and Norwegian acousticians who met in Murmansk recommended that a higher target strength value should be applied for Arctic cod, viz. TS = 21.8 logl 72.7 (Mamylov et al. 1989). The scientists responsible for the survey in autumn 1988 considered this advice, but maintained that the old value should be used until further evidences in favor of the new value could be demonstrated. This view has been maintained every year after, until in 1995, when the estimate was given based on both the old and the new TS value. It was felt that, since the Russian fishing fleet had shown renewed interest in fishing on this resource, the stock size estimates given should be as realistic as possible. It was also decided to recalculate the whole time series of acoustic Arctic cod stock abundance estimate based on the new target strength value. These new estimates are presented in this paper. When estimating the spawning stock in number and weight, a spawning length of 13.0 cm was used, based on unpublished maturity studies at PINRO, Murmansk. All individuals above this length were assumed to belong to the spawning stock (Tables 1-10). Results The acoustic stock size estimation tables for the period are given in Tables For years before 1986, two sources of stock size estimates are available. In the period between 60,000 and 350,000 metric tons of Arctic cod were landed by a Norwegian and Russian fleet. Based on age-distributed catch in numbers from that period,

33 Forage Fishes in Marine Ecosystems 489 Table 1. Stock size estimate of Barents Sea Arctic cod (Boreogadus saida) in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,141 1, ,580 1, ,583 2, , , ,707 3, , , , , , , , , , , , TSN (10 6 ) 24,038 6,263 1, ,441 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 181 4,122 1, ,422 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

34 490 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Table 2. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight , , , , , , , , , , , , , , , , , , , , , , TSN (10 6 ) 15,041 10,142 3, ,333 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 262 8,290 3, ,620 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

35 Forage Fishes in Marine Ecosystems 491 Table 3. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight TSN (10 6 ) 4,314 1, ,562 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 55 1, ,827 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

36 492 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Table 4. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,796 1, ,705 2, ,395 2, , , , , TSN (10 6 ) 13,540 1, ,613 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 1,944 1, ,836 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

37 Forage Fishes in Marine Ecosystems 493 Table 5. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight TSN (10 6 ) 3,834 2, ,799 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 409 2, ,161 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

38 494 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Table 6. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,017 1, ,211 2, ,477 2, ,070 3, , , , , , , , , , , , , , TSN (10 6 ) 23,670 4,159 1, ,903 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 1,626 2,727 1, ,279 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

39 Forage Fishes in Marine Ecosystems 495 Table 7. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,180 1, , , , , , , , , , , , , , , , , , , , ,671 1, , , , , , , TSN (10 6 ) 22,902 13, ,790 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 59 12, ,788 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

40 496 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Table 8. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,132 1, ,061 1, , , , , , , ,229 1,112 3, , , ,246 2, , , , ,536 1, , , , , , , , , , , TSN (10 6 ) 16,269 18,919 2, ,300 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 58 14,159 2, ,329 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

41 Forage Fishes in Marine Ecosystems 497 Table 9. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,403 1, ,299 2, ,046 3, , , , , , , , , , , , , , , , ,525 1, , , , , TSN (10 6 ) 27,466 9,297 5, ,597 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 188 7,089 5, ,067 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

42 498 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Table 10. Stock size estimate of Barents Sea Arctic cod in autumn Age (year class) Sum Biomass Mean Length (10 3 tons) weight ,714 2, , , , , , , , , , , , , , , , , , TSN (10 6 ) 30,697 6,493 1, ,975 TSB (10 3 t) Mean length (cm) Mean weight (g) SSN (10 6 ) 805 5,019 1, ,565 SSB (10 3 t) Numbers in millions, biomass in thousand tons. TSN and TSB are total stock numbers and biomass, respectively, and SSN and SSB are spawning stock numbers and biomass. Mean length (cm) and weight (g) refer to the total stock. Numbers based on TS = 21.8logL 72.7.

43 Forage Fishes in Marine Ecosystems 499 Table 11. Estimated number of Arctic cod individuals at ages 1, 2, and 3 of the year classes (millions) and corresponding instantaneous total mortality coefficient Z. Year class Age 1 24,038 15,041 4,314 13,540 3,834 23,670 22,902 16,269 Age 2 10,142 1,469 1,777 2,221 4,159 13,992 18,919 9,297 Age , ,965 5,044 1,610 Z Z Figure 2. Arctic cod stock size estimates (total biomass) from three different periods. See text for explanation.

44 500 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Monstad and Gjøsæter (1987) presented stock size estimates calculated by virtual population analysis (VPA; Fry 1957). From 1981 up to 1985, the eastern component of the Arctic cod stock was assessed by acoustic methods during Russian surveys in autumn (Unpubl. data, PINRO, Murmansk). These estimates do not cover the whole stock, and must be regarded as minimum estimates only. The results from these surveys (total biomass) as well as those from the period after 1986 (joint surveys) are shown in Figure 2. According to these results, the size of the Barents Sea Arctic cod stock fluctuated considerably in the period Comparing the estimates based on VPA with those based on acoustic surveys, and comparing the acoustic surveys of the eastern component of the stock with those of the total stock may not be totally valid. However, the majority of the stock is normally found in the eastern areas during late autumn, and consequently the acoustic estimates from the period prior to 1986 probably account for the bulk of the stock. Also, both the VPA estimates and the acoustic estimates are meant to be absolute estimates of stock size. According to these data the stock was very large around 1970, but was drastically reduced afterwards. It had increased somewhat in 1981 but was reduced in and again in The bulk of the stock (in numbers) consists of the 1-year-olds (Tables 1-10), and consequently the size of the recruiting year class has a large effect on the total stock size. Seemingly, the year classes 1985 and 1990, 1991, 1993, and 1994 were strong, while the others were at or below average size. The estimated number of fish in consecutive years of the year classes are shown in Table 11. The reduction in number from age 1 to age 3 is considerable. In the 1980s, practically no commercial fishing took place on this stock, and the measured reduction in number of fish in a year class is an estimate of natural mortality. Table 11 gives the estimated total instantaneous mortality coefficient Z per year based on these acoustic estimates, according to the definition: Ni + 1 Z = -1n N (4) i Judged from the mortality estimates obtained, the acoustic estimates of the year classes 1988 and 1989 must have been underestimated as 1- and 2-year-olds in 1990, and/or overestimated as 2- and 3-year-olds in The mortality estimate from age 1 to 2 of the 1991 year class is also unexpectedly low. Excluding these totally unrealistic values, the mean total mortality in the period is 1.16 for age 1-2 and 1.67 for age 2-3. Discussion The acoustic stock size estimation technique is widely used to estimate the abundance of fish which are conveniently located, i.e., not too close

45 Forage Fishes in Marine Ecosystems 501 to the surface or the bottom (MacLennan and Simmonds 1992). The Arctic cod falls in the boundary region of this category of fishes; it is normally classified as semipelagic, forming schools or dense layers which sometimes extend down to the bottom. The TS value to use for Arctic cod is difficult to choose, because experimental work on target strength measurements for this species is limited. The value used up to now on the Barents Sea Arctic cod stock was probably too low, but the current chosen value (Mamylov et al. 1989) should also be regarded as tentative. The goodness of the stock size estimates presented here is difficult to judge. The main source of error, in addition to the not-well-documented TS value, is probably incomplete coverage of the stock. This will lead to a varying amount of underestimation of stock size. This problem is partly known (and mentioned in the survey reports) but some years there may have been significant parts of the stock residing outside the surveyed area disregarding the fact that the stock was seemingly totally covered. Problems with incomplete coverage were mentioned every year, but seem to have raised particular concern in 1987, 1990, and The mortality estimates based on the acoustic stock size estimates are high compared to most other species in this area, and probably reflect this stock s position as a forage fish, being a feeding object of most of the predatory stocks living in the Arctic (Klumov 1937). It serves as food for marine mammals, fish, and birds throughout most of its distribution area. The main consumers of Arctic cod are seals (mainly harp seals, Phoca groenlandica, and ringed seals, P. hispida) and white whales (Delphinapterus leucas). Harp seals are known to feed on Arctic cod during autumn in the northern areas as well as along the coasts of Novaya Zemlya in winter (Nilssen 1995). During the spawning migration the Arctic cod is normally followed by aggregations of seals and white whale. Migration and approaches of harp seals to the sites of reproduction in the White Sea are considered to be determined by peculiarities of the prespawning and spawning Arctic cod distribution (Pechenik et al. 1973). Arctic cod, mainly of ages 1 and 2, is a principal prey species for seabirds in pelagic, ice-covered waters in the Spitsbergen region (Mehlum and Gabrielsen 1993) as well as in other parts of the Barents Sea (Mehlum and Gabrielsen 1995). During summer and autumn Arctic cod are of essential importance in feeding of Atlantic cod (Gadus morhua), Greenland halibut, and haddock in the feeding areas (Nizovtsev 1975, Kovtsova 1990). In a paper presented at this symposium by Bogstad and Mehl (1997), the yearly consumption of Arctic cod by Atlantic cod was estimated to vary from 3,000 to 803,000 metric tons in the period , constituting % of the total food consumed by Atlantic cod. The consumption of Arctic cod was significantly higher in the periods and after 1992 compared to the other years in the studied period. In Figure 3 the estimated consumption by cod is

46 502 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Figure 3. The estimated consumption of Arctic cod (Boreogadus saida) by Atlantic cod (Gadus morhua) (Bogstad and Mehl 1997) compared to the total mortality of Arctic cod (the total reduction in estimated numbers of age groups 1-2 and age groups 3-4 in a particular year). The mortality values for 1990 and 1991 have been removed (see text for explanation). compared to the estimated total mortality of Arctic cod (total reduction in numbers of fish from age 1 to 2 and from age 2 to 3 in a particular year). Keeping in mind that the mortality estimates based on the acoustic stock size estimates in 1989 and particularly in 1991 are probably too low, while the opposite is probably the case in 1990, there is a fairly good correspondence between the two curves in Figure 3, which indicates that consumption by cod is a major source of mortality on the Arctic cod stock. References Bodholt, H., H. Nes, and H. Solli A new echo-sounder system. Proc. IOA (International Organization of Acoustics) 11(3): Dommasnes, A., and I. Røttingen Acoustic stock measurements of the Barents Sea capelin A review. In: H. Gjøsæter (ed.), Proceedings of the Soviet-Norwegian Symposium on the Barents Sea Capelin, Bergen, Norway, August Institute of Marine Research, Bergen, pp

47 Forage Fishes in Marine Ecosystems 503 Foote, K.G., H.P. Knudsen, R.J. Korneliussen, P.E. Nordbø, and K. Røang Postprocessing system for echo sounder data. J. Acoust. Soc. Am. 90(1): Foote, K.G., H.P. Knudsen, G. Vestnes, D.N. MacLennan, and E.J. Simmonds Calibration of acoustic instruments for fish density estimation: A practical guide. ICES Coop. Res. Rep. 144, 57 pp. Fry, F.E.J Assessments of mortality by use of virtual populations. Joint Scientific Meeting of ICNAF, ICES and FAO on fishing effort, the effects of fishing of resources and the selectivity of fishing gear. Contribution No. 15. Gjøsæter, H., and V. Anthonypillai Utbredelse av polartorsk i Barentshavet (Distribution of Arctic cod in the Barents Sea). Fisken Havet 23, 56 pp. (In Norwegian with English summary.) Gjøsæter, J Preliminary results of Norwegian polar cod investigations Int. Counc. Explor. Sea Counc. Meet. 1973/F:8, 23 pp. Klumov, S.K Arctic cod and its importance for some vital processes of the Arctic Ocean. USSR Academy of Sciences, No. 1. Kovtsova, M.V Flatfishes of the Barents Sea and adjacent waters. In: Biological resources of the shelf and marginal seas of the USSR. Nauka Press, Moscow, pp MacLennan, D.N., and E.J. Simmonds Fisheries acoustics. Chapman and Hall, London. 325 pp. Mamylov, V.S., N.G. Ushakov, M.S. Shevelev, L.I. Serebrov, A.E. Dorchenkov, E.N. Fimina, and N.I. Efimov Metoditsjeskie rekomendatsii po provedeniju mnogovidovoi tralovo-akustitsjeskoi semki (Methodological recommendations for the multispecies trawl-acoustic surveys). PINRO, Murmansk. 119 pp. (In Russian.) Mehlum, F., and G.W. Gabrielsen The diet of high-arctic seabirds in coastal and ice-covered, pelagic areas near the Svalbard archipelago. Polar Res. 12(1):1-20. Mehlum, F., and G.W. Gabrielsen Energy expenditure and food consumption by seabird populations in the Barents Sea region. In: H.R. Skjoldal, C. Hopkins, K.E. Erikstad, and H.P. Leinaas (eds.), Ecology of fjords and coastal waters. Elsevier, Amsterdam, pp Monstad, T., and H. Gjøsæter Observations on polar cod (Boreogadus saida) in the Barents Sea Int. Counc. Explor. Sea. Counc. Meet. 1987/G:13, 24 pp. Nakken, O., and A. Dommasnes The application of an echo integration system in investigations on the stock strength of the Barents Sea capelin (Mallotus villosus, Müller) Int. Counc. Explor. Sea Counc. Meet. 1975/B:25, 20 pp. Nakken, O., and A. Dommasnes Acoustic estimates of the Barents Sea capelin stock Int. Counc. Explor. Sea Counc. Meet. 1977/H:35, 10 pp.

48 504 Gjøsæter & Ushakov Acoustic Estimates of Barents Sea Arctic Cod Nilssen, K.T Seasonal distribution, condition and feeding habits of Barents Sea harp seals. In: A.S. Blix, L. Walløe, and Ø. Ulltang (eds.), Whales, seals, fish and man. Elsevier, Amsterdam, pp Nizovtsev, G.P On feeding of Greenland halibut Reinhardtius hippoglossoides (Walbaum) in the Barents Sea. CNIITEIRKH, Moscow, No. 44, 44 pp. (In Russian.) Pechenik, L.N., V.P. Ponomarenko, and L.I. Shepel Biologiya i promysel sayki Barentseva morya (Biology and fishery of Arctic cod in the Barents Sea). Pishchevaya promyshlennost. 68 pp. (In Russian.)

49 Proceedings Forage Fishes in Marine Ecosystems 505 Alaska Sea Grant College Program AK-SG-97-01, 1997 Abundance and Distribution of Northern Anchovy Eggs and Larvae (Engraulis mordax ) off the Oregon Coast, Mid-1970s vs and 1995 Robert L. Emmett, Paul J. Bentley, and Michael H. Schiewe National Marine Fisheriees Service, Northwest Fisheries Science Center, Seattle, Washington Extended Abstract Northern anchovy (Engraulis mordax) is one of the most abundant fish species in the California Current and is a major prey for many species of fish, seabirds, and marine mammals off the Oregon and Washington coast. Egg and larval fish surveys in the 1970s (Richardson 1981) revealed that the northern subpopulation of northern anchovy residing off Oregon and southern Washington spawned primarily in July in an offshore area centered just south of the Columbia River mouth and offshore km. Using an egg production method, Richardson (1981) estimated minimum northern anchovy spawning biomasses for this population in 1975 and 1976 were 262,506 and 144,654 metric tons, respectively. Coincidentally, marine survival of coho salmon smolts which out-migrated in 1975 were high and those of 1976 relatively low, in the Oregon Production Area (Nickelson 1986). The objective of our research is to identify the status of the northern anchovy population off Oregon and southern Washington and investigate the relationship between anchovy abundance and juvenile coho salmon ocean survival. To accomplish this task, eggs and larvae of northern anchovy were collected using a vertically towed 25-cm-diameter bongo (CalVET) net constructed of 0.15-mm mesh and deployed from the National Marine Fisheries Service (NMFS) 17.4-m research vessel Sea Otter. At each station, the net was deployed to a depth of 70 m (or just above the bottom) and retrieved at a rate of 70 m per minute. Samples were preserved in a 4% buffered formaldehyde solution. Other Robert Emmett is also associated with the Department of Fish and Wildlife, Oregon State University, Corvallis, Oregon.

50 506 Emmett et al. Northern Anchovy off the Oregon Coast parameters measured included profiles of temperature, conductivity, and depth. Seawater samples were taken at each station at a depth of 3 m, filtered, and frozen for later chlorophyll a analysis. Ichthyoplankton samples were collected during July 1994 and 1995 off southern Washington and northern Oregon; July is the peak month of spawning for northern anchovy in the Pacific Northwest (Richardson 1981). A total of 234 stations along 12 east-west transects were sampled in 1994 and 121 stations were sampled in Transects extended from 9 to 190 km offshore and were located about 32 km apart. Each transect consisted of up to 20 evenly spaced sampling stations. The July 1994 and 1995 ichthyoplankton collections revealed that the abundance and distribution of northern anchovy eggs and larvae were extremely limited when compared to those observed in the mid- 1970s (Figure 1). In 1994, we found northern anchovy eggs at only one station (0.4% of all stations sampled) located 18 km west from the Columbia River mouth (Figure 1B). Calculated egg densities were 400 eggs per 10 m 2 at this station. In 1995, we found egg concentrations as high as 5,600 per 10 m 2 at one station (Figure 2). However, during both years, eggs, and thus spawning, occurred nearshore on the continental slope. Richardson (1981) found concentrations of anchovy eggs as high as 17,931 per 10 m 2 and 5,777 per 10 m 2 during 1975 and 1976, respectively, over a broad area off the continental slope and associated with the Columbia River plume. Although the 1994 and 1995 distribution of larval northern anchovy was somewhat similar to the 1970s (i.e., offshore in the Columbia River plume), they were markedly less abundant than in historical surveys. In 1994, we found only two larvae that were positively identified as northern anchovy at two stations. An additional 18 clupeiform larvae were in poor condition and could not be identified. Even including these unidentified larvae as possible northern anchovy larvae, larval densities were much lower in July 1994 and 1995 than off Oregon in 1975 or 1976 (Richardson 1981) or during 1983 (Brodeur et al. 1985), an El Niño year. Assuming that all the identified clupeiform larvae were northern anchovy, the highest larval anchovy density we observed was 1,000 per 10 m 2 at one station in Richardson (1981) found higher larval anchovy densities during both 1975 and She also found northern anchovy larvae at 47% and 57% of her sampling stations, respectively. In contrast, we noted larval anchovy at only 5% of our stations in 1994 and 9% in Further, anchovy larvae were relatively rare in July 1994 and 1995, numerically less than 10% of all larvae collected. This differs markedly from Brodeur et al. (1985), who observed that northern anchovy was the dominant larval fish collected in 1983, accounting for half of all larval fish collected. We have not yet estimated spawning biomass, but these data indicate that northern anchovy spawning biomass in 1994 and 1995 was

51 Forage Fishes in Marine Ecosystems 507 Figure 1. Location and density of northern anchovy eggs and larvae found in July 1976 (A) (from Richardson 1981) and July 1994 (B) from ichthyoplankton surveys off Oregon and southern Washington. Actual numbers of eggs and larvae captured in 1994 are shown in B. In 1994, larvae included some unidentified clupeid larvae that could have been northern anchovy or Pacific sardine. low, indicating that the northern subpopulation of northern anchovy has probably declined in abundance. Regardless of the specific factors that caused this apparent decline, the consequences for other living marine resources dependent on this species as prey are probably significant. Although there is some indication that Pacific sardines (Sardinops sagax) may be increasing in abundance and occupying the same niche presently occupied by northern anchovy off Oregon (Bentley et al. 1996), there is no evidence that sardines are an important prey of predators which typically consume northern anchovy. Most migrating juvenile salmonids enter the ocean at approximately the same length as adult anchovies. A severe reduction in the anchovy populations off the Pacific Northwest coast could result in increased predation rates on salmonids if no alternative baitfish or invertebrate prey is available. We are currently investigating this possibili-

52 508 Emmett et al. Northern Anchovy off the Oregon Coast Figure 2. Distribution and abundance of northern anchovy eggs and larvae captured off Oregon and southern Washington during a July 1995 ichthyoplankton survey. ty in a pilot-scale study of the distribution and stomach contents of piscivorous fish near the mouth of the Columbia River. References Bentley, P.J., R.L.Emmett, N.C.H. Lo, and H.G. Moser Egg production of Pacific sardine (Sardinops sagax) off Oregon in Calif. Coop. Oceanic Fish. Invest. Rep. 37: Brodeur, R.D., D.M. Gadomski, W.G. Pearcy, H.P. Batchelder, and C.B. Miller Abundance and distribution of ichthyoplankton in the upwelling zone off Oregon during anomalous El Niño conditions. Est. Coast. Shelf Sci. 21: Nickelson, T.E 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(3): Richardson, S.L Spawning biomass and early life of northern anchovy, Engraulis mordax, in the northern subpopulation off Oregon and Washington. U.S. Natl. Mar. Fish. Serv. Fish. Bull. 78(4):

53 Proceedings Forage Fishes in Marine Ecosystems 509 Alaska Sea Grant College Program AK-SG-97-01, 1997 The Eulachon (Thaleichthys pacificus) as an Indicator Species in the North Pacific D.E. Hay and J. Boutillier Department of Fisheries and Oceans, Pacific Biological Station, Nanaimo, British Columbia, Canada M. Joyce Department of Fisheries and Oceans, Annacis Island, New Westminster, British Columbia, Canada G. Langford Geo-Spatial Systems Ltd., Nanaimo, British Columbia, Canada Abstract Eulachons (Thaleichthys pacificus) were captured incidentally in annual shrimp trawl surveys conducted off the coast of southern British Columbia. We compiled these catch records and used spatial analysis to estimate eulachon densities. From this we derived an offshore index of abundance for nearly all years from 1973 to We compared the offshore index data with catch data from the Columbia and Fraser rivers. The offshore index is significantly correlated to eulachon catch records in the Columbia River but not with the Fraser River. In both rivers, however, there were sharp declines in This sharp decline was observed in the previous year (1993) in the offshore index. Declines in 1994 spawning runs also happened in some smaller rivers in British Columbia but no time series data are available. The offshore index time series appears to be influenced by the time trends in ocean climate, but in ways that we cannot explain. The offshore index varied positively with water temperature (sea surface temperature was used from Amphitrite Point, on the west coast of Vancouver Island). Fraser River varied negatively in relationship with temperature but there was no apparent relationship between Columbia River catches and temperature. There was, however, positive covariance between offshore index and Columbia River catches. Therefore, we found three relationships: (1) Fraser River catches were negatively related to temperature, (2) offshore eulachon

54 510 Hay et al. Eulachon as an Indicator Species in the North Pacific abundance was positively related to temperature, and (3) the Columbia River catch was correlated with the offshore index. Although each relationship was statistically significant, we are less certain of the biological significance. The clearest results were the sharp declines in 1983 and The 1983 offshore decline preceded a sharp Columbia River catch decline by 1 year. The 1993 offshore decline preceded a widespread decline in most rivers, including the Columbia and Fraser, where eulachons are known to spawn even though the timing of the spawning runs varies by 2-3 months. Synchronous (i.e., within a year) changes among different eulachon populations may reflect geographically widespread oceanographic changes (El Niño). In the rivers, there may be other, more localized, environmental changes affecting eulachons, particularly changes affecting spawning areas. Introduction In the last 80 years, the eulachon (Thaleichthys pacificus) has had a relatively low profile among the fisheries of the Pacific coast. This was not always the case. In the last century, the eulachon was much better known, mainly because of its importance among the coastal Aboriginal cultures (Hart 1973, Stewart 1975, Kuhnlein et al. 1981). In particular, it was an extremely important source of food, and a vital cultural and economic commodity among coastal communities. The remarkable characteristic about eulachons was its high lipid content, so high that it is possible to ignite the tail of dried specimens and have the carcass burn like a candle. Oil, or grease derived from the eulachon was so important as a trading commodity in Aboriginal society that extensive transport trails throughout the coast were known as grease trails. The rendering of the fish to grease took on enormous significance and the technology developed variations among different societies. Therefore, for centuries, and perhaps millennia, the variations in the distribution and abundance of eulachons have been under intense observation and scrutiny among people living in coastal communities. The eulachon has supported small commercial fisheries on the Columbia and Fraser rivers for most of this century (Anon. 1993, Hart 1973). There was a relatively large commercial fishery for eulachons on the Nass at the turn of the century. This has changed so that, except for the Fraser River, the present fisheries are mainly conducted by Aboriginal people for the production of grease and as a source of food. In the 1940s and 1950s, the commercial fishery on the Fraser River was a source of food for fur animals and for small markets for human consumption. The price was not high for this product and thus its lack of commercial value probably accounts for the very little attention and concern paid to this species. In the last decade, several developments changed that. The important run of eulachons in the Kitimat River (near the city of Kitimat, B.C.,

55 Forage Fishes in Marine Ecosystems 511 at the head of Douglas Channel) was impacted from industry and urbanization; the size of the spawning runs were reduced and the spawning fish chemically altered by effluent so that they became unpalatable. Other potential industrial changes were considered on other rivers. Further, any impact of forestry, particularly as it might affect the hydrology of spawning streams, has not been thoroughly investigated. Concurrently, there were changes in the marine environment, with the development of industrial trawl fisheries, and eulachons have long been known to be part of the discarded bycatch. Finally, there have been some striking changes in ocean climate, and any effects of this on eulachons are not known. This paper presents an analysis of eulachon catch data collected incidentally during offshore surveys, and compares that with catch data from the Columbia and Fraser rivers. We also examine the effect of changes in ocean temperature on the changing size of the spawning runs, or catches, in the rivers. We use these analyses to comment on the effect of ocean climate on eulachon populations. First, however, we present a brief review of eulachon distribution and biology because this basic information is not readily available in the scientific literature. Brief review of eulachon distribution and biology Eulachons are small (>25 cm) silver fish, one of about 12 species in the family Osmeridae (McAllister 1963). They resemble small salmon, with an adipose fin and extended anal fin. Although age determination is not well established, rings on otoliths indicate that ages of 5-6 are probably near maximal. The age of sexual maturity also is uncertain, but it may be about age 3. It is not known if eulachons die following spawning (like salmonids) although substantial postspawning mortality has been observed in many rivers. Eulachons spawn in late winter and early spring, beginning in January and February in the Columbia River and extending to late April and May in northern rivers. It seems that most spawning occurs in fresh water, but usually not far above the upper extent of seawater (Langer et al. 1977). The eggs are small (<1.0 mm diameter) and are mildly adhesive (Hart and McHugh 1944). Incubation is temperature-dependent (Smith and Saalfeld 1955), but at ambient temperatures of 4-5 C, hatching occurs in about 3 to 4 weeks. The larvae are small (5-8 mm). In most rivers the larvae are flushed to sea rapidly, probably within minutes in some streams. Once in the sea, the distribution and biology of larval and juvenile eulachons is unknown, and they do not occur commonly in samples of other species. Specimens sometimes occur, however, in guts of predatory species and in catches of some midwater and offshore trawl samples. There are limited suitable spawning rivers, and virtually all have continental drainages that produce freshets in the spring. Eulachons do not seem to regularly spawn in the smaller coastal rivers that produce fall freshets which are characteristic of the rivers and streams of the

56 512 Hay et al. Eulachon as an Indicator Species in the North Pacific coastal islands. For instance, there are no established eulachon spawning populations on any of the coastal islands such as Vancouver Island, the Queen Charlotte Islands, or any of the islands in southeastern Alaska. Although the exact distribution of eulachon populations is not well documented, it appears that the number is not large. Eulachons seem to be abundant in the southern Bering Sea, the northern extent of the range. They also occur in Cook Inlet drainages. In southeastern Alaska they are reported to occur in the Unik, Smeaton Bay, Bradfield, Stikine, Kenai, Yakutat, and Taku (Pers. comm., Alaska Department of Fish and Game). In northern British Columbia they occur in the Nass and Skeena rivers. In Douglas Channel and Gardner Canal they occur in a number of different small rivers including the Kitimat, Kildala, Kemano, Kitlope, Kowesas, and perhaps several others. In central British Columbia, important runs occur (or occurred) in the Bella Coola River, Owikeno River, and rivers at the heads of various inlets, such as Kingcome, Knight, and Bute inlets. In total, in British Columbia there are at least 12, and perhaps 20, spawning runs of varying sizes. In contrast, there probably are about 10,000 different runs, or populations, of salmonids over the same range. The total range of eulachons appears to be confined to rivers (particularly glacier-fed rivers) draining western North America. Therefore, the total number of rivers that support eulachons, throughout their entire range, may not exceed 30. Methods Data sources We used four different data sets in this paper. (1) Offshore abundance data was derived from analyses of bycatch in annual surveys of shrimp off the west coast of Vancouver Island. The data and analyses are reported here for the first time and the methods are described below. (2) We assembled catch data from the Fraser River, based on Canada Department of Fisheries and Oceans (DFO) catch statistics and manuscript reports (Ricker et al. 1954). These catch data probably are only a rough approximation of total abundance and are affected by omissions in the catch records and catch declines that reflect markets more than abundance. (3) We use Columbia River eulachon catch data, from 1934 to 1993, as reported in published reports from the Washington and Oregon departments of fish and wildlife (Anonymous 1993). Data for more recent years was obtained though personal contact with Washington State fisheries personnel (Pers. comm., S. Hawkins). These data are approximate representations of the spawning biomass of eulachons (or Columbia River smelt, as they are called there) although there is a substantial recreational fishery, or personal use fishery, that is not included in the catch data we use. (4) We use ocean temperature data collected from the lighthouse at Amphitrite Point, near Barkley Sound, on the west coast of Vancouver Island. This is the closest source of temperature data to the

57 Forage Fishes in Marine Ecosystems 513 location of the shrimp surveys. The general locations of the offshore catches, Amphitrite Point on the west coast of Vancouver Island, and the Fraser and Columbia rivers are shown in Figure 1. No systematic eulachon catch data have been assembled from other rivers. However, it was established that the catches in the Klinaklini River, at the head of Knight Inlet, were abnormally low in In the same year, the runs appear to have been lower in the Kemano River (Pers. comm., Adam Lewis, Triton Consultants) and the Skeena (Pers. comm., Tom Pendray, DFO), although there are no quantitative data that document this. The spawning runs and Aboriginal fishery in the Nass River, at the extreme northern part of British Columbia, did not appear to change in that year. Fishing gear For most years, biomass trawl surveys were conducted in early May off the west coast of Vancouver Island (Figure 1). Usually more than 50 tows were made during each survey. Two standardized trawls were used. During , a 21.3-m semi-balloon Gulf of Mexico shrimp otter trawl was used. The net was rigged with a light groundline of plastic and rubber rollers attached to the footrope of the net. From 1977 to the present, the net used for the survey was a standard 18.6-m, National Marine Fisheries Service (NMFS) high-rising, shrimp-sampling otter trawl (Boutillier et al. 1977). Comparison tows were carried out in 1977 between the two trawls. The NMFS trawl was 1.4 times more efficient. These results were comparable to results from similar comparisons conducted by NMFS (Cruise Report Cruise No NOAA R/V Oregon). Trawl locations for the biomass survey were established using a systematic grid pattern based on Loran C blocks. Tows were made diagonally through adjacent 5900-Z 10-microsecond blocks along successive 5900-Y lines, 20 microseconds apart. Tow duration, except when nets fouled, was 30 minutes and positions were recorded to the nearest 0.1 nautical miles (nmi). The distance covered depended on tide wind conditions, but most varied between 1.0 and 1.7 nmi with a mean of 1.39 nmi (Boutillier et al. 1990). Catch analyses The catch from each trawl catch was dumped on deck. Large species were sorted, weighed, and discarded. The balance of each catch, consisting of shrimp, small fish (including eulachons), and other invertebrates, was shoveled into baskets and weighed. One or two baskets of this mixed catch were then sorted and weighed by species to determine the proportional catch composition by species. The calculated percentage of species by weight was then used to extrapolate the total weight of each species in the catch. In 1995 we started a more intensive analysis of eulachons including estimates of length, weight, and age. Preliminary results, which are not presented here, indicate there may be several different year classes of eulachons in the catches.

58 514 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 1. Locations of offshore catches, Amphitrite Point on the west coast of Vancouver Island, and the Fraser and Columbia rivers.

59 Forage Fishes in Marine Ecosystems 515 Survey design, biomass index, and time series Biomass abundance indices were calculated by modeling the catch data over the area sampled using geographic information system (GIS) software (Compugrid ) that supported a bicubic spline interpolation procedure. For this analysis, the Tofino ground survey area (Figure 1) was defined as a rectangular area starting at longitude and latitude extending 50 nm north (322 True) and 15 nm west (52 True). This represents a rectangle of about nmi (750 nmi 2 ) or km (2,430 km 2 ). For GIS analyses, the area was divided into square cells or hectares (ha), each measuring 100 m on a side or 10,000 m 2 /cell. The towable area, within this larger area, was bounded by a set of non-towable boundary points that were determined from previous surveys. The calculation of the biomass index assumes that all the towable area within the boundary (g/m 2 or tons/km 2 ) in the cell by using the catch data obtained in a tow which had its midpoint within the cell. In the case of repeated tows, the mean of the two tows was used as the value for the cell corresponding to the location of the center point of the tow. The bicubic spline interpolator was used to fill blank grid cells with interpolated values. Figure 2 shows some representative years of the survey and indicates interpolated isopleths of uniform density within the grid. The total biomass and areas of concentration were calculated by summing the values (for all values >0) of the grid cells within the survey area. A condensed example for a single year, showing 10 density classes from 0.1 to g/m 2, is shown in Table 1. For each survey from 1973 to 1996 (except for some missing years) the biomass was estimated as the sum of the cell-specific densities. For convenience, we express the abundance in tons, or in tons/km 2 (units are same as g/m 2 ) but we advise that these are relative and not necessarily absolute estimates of density and biomass. Results The data: Offshore biomass and density, river catches, and ocean temperatures The time series of offshore abundance, shown as an abundance index is in Table 2. Also shown are Fraser River and Columbia River eulachon catches and the ocean temperatures, shown as the daily mean for the three (spring) months of March to May, from Amphitrite Point. Estimates of change in offshore abundance ( ) Changes in offshore eulachon abundance (Figure 2) show selected years of eulachon distribution and abundance off Barkley Sound on the west coast of Vancouver Island. Of particular note are the smaller and more

60 516 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 2A-F. Six representative years of the offshore shrimp surveys. The contours show areas of uniform density based on the sizes of catches in shrimp trawl catches. The sums of the areas of uniform density were used to estimate an annual biomass index, shown in Table 1. Figure 2A. Figure 2B.

61 Forage Fishes in Marine Ecosystems 517 Figure 2C. Figure 2D.

62 518 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 2E. Figure 2F.

63 Forage Fishes in Marine Ecosystems 519 Table 1. Example of estimation of the biomass index for The cumulative biomass from all cells is the biomass index. Biomass Cumulative Cumulative Number in class biomass Area area Biomass class of cells (tons) (tons) (km 2 ) (km 2 ) , , , , , , , , , , , , , , , , , , Total 199,346 2, , , , In this example, there were 56,040 cells (or hectares) with an estimated density of g/m 2 for a total of tons (or a mean density of 1.02 g/m 2 in that biomass class). The last two columns indicate the sum of the area per biomass class and the cumulative area (km 2 ) for the 1992 survey. The number of biomass classes is reduced for brevity.

64 520 Hay et al. Eulachon as an Indicator Species in the North Pacific Table 2. Fraser River catch, offshore index, Columbia River catch, and sea surface temperature at Amphitrite Point. Fraser River Offshore Columbia River Temperature Year catch (tons) index (tons) catch (tons) ( C) Apr-Jun , , , , , , , , , , , , , , , , , , , , , , , , , , The annual estimated eulachon catches (tons) from the Fraser and Columbia rivers (columns 2 and 4). The 1995 and 1996 data are preliminary. The offshore biomass index in tons (column 3) was first estimated from Temperature is the mean sea surface temperature at Amphitrite Point from April to June. For brevity, the early years ( ) are not shown.

65 Forage Fishes in Marine Ecosystems 521 geographically restricted distributions in 1983 and The data in Table 1, showing the biomass index, were derived from spatial analyses of the catch data (see Table 1). Temporal changes in Fraser and Columbia river catches Fraser River catches have declined since the 1940s and 1950s (Figure 3). In part the downward trend in Figure 3 may reflect changing markets and incomplete catch data, but there is little doubt that total annual eulachon abundance is lower in recent years. The two most recent years, 1995 and 1996, are based on recent improvements in collection of catch data and we believe they are accurate. In the last 60 years, Columbia River eulachon catches are approximately 5 times greater than those from the Fraser River and, except for the last 5 years, show no apparent decrease with time (Figure 4). There was a period of consistently lower catch in the 1960s followed by an increase in the 1970s and 1980s. The low point in 1984 is noteworthy. This point follows 4 years after the volcanic eruption on Mt. St. Helens. Volcanic ash contaminated the main eulachon spawning area in the lower Columbia system (Cowlitz River) and some opinion holds that this disrupted spawning success resulted in poor recruitment 4 years later. There is no explanation for the recent decrease in catches and abundance. An additional or alternate explanation is that the 1993 El Niño event disrupted the eulachon population, either by a change in numbers or a change in distribution. If so, the 1983 El Niño may have negatively impacted the 1984 spawning run. Comparison of river data with offshore data The offshore biomass index data when plotted with Columbia River catch data (Figure 5A) show very similar trends in time, particularly since the mid-1980s. The biomass index showed a low point in 1983, one year prior to the low point in the Columbia River catch. The actual difference in time, however, was only about 8 months because the offshore surveys were made in May and eulachon spawn, in the Columbia River, from January to March. The offshore biomass index when plotted against Columbia River catches (Figure 5B) shows a strong positive correlation (r 2 = 0.34, P<0.01). Nonlinear plots have even higher correlations but the main point of the regression is to show that there is significant positive covariance between the two data sets. The offshore biomass index when plotted against the Fraser River catches (Figure 5C) shows no significant trend. The catches of the Fraser and Columbia rivers show no significant covariation (Figure 5D). What is not apparent from this comparison, however, is the fact that both rivers had extremely low abundances of

66 522 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 3. Annual catches of eulachons in the Fraser River. The low catches from 1970 to the present may reflect limited markets, but abundance was particularly low in Figure 4. Annual catches of eulachons in the Columbia River. The commercial catches probably reflect changes in abundance. The catches in 1984 and 1994 were particularly low.

67 Forage Fishes in Marine Ecosystems 523 Figure 5A. Comparison of the offshore biomass index (solid line) with the Columbia River eulachon catch (dashed line), by year, Note that the offshore index declined sharply in 1983, one year prior to the low catches in the Columbia River in Since 1990, the trends in the data appear more synchronous. Figure 5B. Regression of the offshore biomass index with Columbia River eulachon catches. The Columbia River eulachon spawn in late winter (January-March) and the biomass index is estimated from surveys in May-June.

68 524 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 5C. Regression of the offshore biomass index with Fraser River eulachon catches. Figure 5D. Comparison of the Columbia River and Fraser River eulachon catches. There is no apparent relationship.

69 Forage Fishes in Marine Ecosystems 525 eulachons in This led to fishing restrictions on both rivers. The observations of low abundance, and the subsequent management actions were made completely independently. Other, smaller rivers in British Columbia had very low returns of spawners in the same year (1994). Effect of temperature There is no significant covariance between temperature (April-June) and the offshore biomass index in the same year (Figure 6A) but there is significant positive covariance between the biomass index of the following year (Figure 6B). If this covariance has any biological significance, it may be that following warmer years, eulachons in offshore areas were more abundant than in cold years. An alternate explanation is that eulachons may change their offshore distribution in cool years and move out of the survey area. There is no covariance between Amphitrite Point temperature and Columbia River catches (Figure 6C). Probably such a relationship would not be expected, because the catches occur prior to the period when the temperatures are used for these analyses. However, even if the data are lagged by one year, or if different combinations of months are used, no apparent relationship was found. There is a strong, negative covariance between Amphitrite Point temperature and Fraser River catches (Figure 6D). The weakest part of this comparison, however, is that the Fraser River catches do not necessarily reflect abundance, so some or all of this covariance could be spurious. Discussion Origin of the offshore eulachons It seems probable that most of the eulachons captured offshore of Vancouver Island spawn in the Columbia River. Based on the approximately 60 years of catch data (Table 1), the Columbia River eulachon population is much larger than the Fraser River population and the consistency of the eulachon bycatch in the offshore waters would probably require a population larger than that of the Fraser. The consistency between the trends in the offshore biomass index and the Columbia River catches (Figures 5A, 5B) also is evidence that the surveys are made on the same population. The phenomenon of southern fish spending their summer months feeding in the productive waters off southern Vancouver Island is known in several species, including hake and sardines (Ware and Mc- Farlane 1989). Therefore, it is not surprising if it occurs in eulachons. Also, there is only a limited number of known eulachon rivers, and most are small. None occurs on Vancouver Island, and the next closest Canadian river is at the head of Knight Inlet, hundreds of kilometers distant. There may be some small eulachon runs in small rivers draining the

70 526 Hay et al. Eulachon as an Indicator Species in the North Pacific Figure 6A. Regression of daily mean sea surface temperature ( C) from April through June at Amphitrite Point with the offshore biomass index for the same year. The regression is not significant. Figure 6B. Regression of daily mean sea surface temperature ( C) from April through June at Amphitrite Point with the offshore biomass index estimated one year later. The correlation is highly significant.

71 Forage Fishes in Marine Ecosystems 527 Figure 6C. Regression of the daily mean sea surface temperature ( C) from April through June at Amphitrite Point with the Columbia River eulachon catches taken in the next year. The regression is not significant. Figure 6D. Regression of the daily mean sea surface temperature ( C) from April through June at Amphitrite Point with the Fraser River eulachon catches taken in the next year. The negative regression is significant but explains relatively little of the catch variation on the Fraser River.

72 528 Hay et al. Eulachon as an Indicator Species in the North Pacific west side of the Olympic Peninsula, but this is not documented. Although the number of established eulachon spawning rivers is very limited, with perhaps 30 (and maybe less than 20) throughout the world range of the species, there is good evidence that eulachons occasionally stray into different, previously occupied rivers. These incidents of straying seem to occur during periods of El Niño or other events, and do not seem to lead to established populations Effects of temperature and other factors on eulachons Two distinct but different temperature effects are: (1) an increase in the offshore abundance with temperature and (2) a decrease in the Fraser River eulachon catch with temperature. These effects appear to be contradictory, because if there really is a greater biomass of eulachons with warmer temperatures, then this effect might be expected to be consistent among populations. If so, Fraser River spawning runs also should increase with temperature. Another explanation, however, is that temperature alters offshore eulachon distribution, and it is conceivable that some eulachons that might have returned to the Fraser River went elsewhere. This explanation, however, would require that the homing fidelity of eulachons is more plastic than that of salmonids. There is, in fact, some evidence to support this. In 1994, the year of an unprecedented low return on the Columbia River, there was a novel eulachon spawning event in the Chehalis River system (in the Wynoochee tributary) where eulachons spawned for the first time (Pers. comm., P. McAllister, Washington State Department of Fisheries). Unpublished correspondence within DFO also reveals that eulachons have spawned once, in 1955, in the Somass River, draining into Alberni Inlet on the west coast of Vancouver Island. Within the lower reaches of the Columbia River there have been large interannual differences in eulachon spawning sites (Delacy and Batts 1963). Also, within the Fraser River, it appears that the range of spawning sites varies through much of the lower 100 km of the river and its tributaries (Samis 1977). An important consideration of eulachon biology concerns the age structure and the age of recruitment to the spawning stock. We know almost nothing of this but this aspect is potentially important to our analyses, especially with respect to the time lag between offshore biomass estimates, temperature effects, and in-river catches. This topic is under current investigation. Another factor is the potential effect of shrimp bycatch, as a factor affecting eulachon populations. We also are starting to examine this issue, both within the study area described in this paper and other areas on the British Columbia coast. The eulachon as an indicator species Within the Columbia River, the eulachon may be one of the few species that has not experienced systematic reductions in abundance, although

73 Forage Fishes in Marine Ecosystems 529 this is not correct for the last few years. Therefore, in this sense, the eulachon is a poor indicator of long-term changes to other species. The recent decline, however, is drastic, and may be an indication of changes in ocean climate. In this sense, it is an indicator species. The problem with the eulachon as an indicator species, however, is that we are not certain exactly what it indicates. High offshore abundances of eulachons occur with higher temperature, and this seems to be reflected in higher Columbia River catches but lower Fraser River catches. If this is correct, then the offshore distribution and abundance of eulachons may be an indictor of potential catches or spawning runs, but the predictions vary according to different river systems. Although eulachons do not support major commercial fisheries, they are nevertheless extremely important for other reasons, specifically their role in Aboriginal utilization and culture. Often, when eulachon runs have been smaller than expected, many local fishers and observers invoke a range of explanations for the cause. Usually these explanations include: spawning habitat disruption, pollution, overfishing, increased predation by mammals and birds, and weather or climate change. Many of these explanations appear to have substance, especially those directed at spawning habitat impacts and particularly on the lower Fraser River. There, active dredging has occurred during eulachon spawning season, in their spawning areas. There are many other potentially harmful factors, including impacts from logging. It would be imprudent, however, not to include broad-scale effects, such as changes in ocean climate, as part of the explanation for changes in eulachon abundance or distribution. The challenge for the future conservation of eulachons will be to evaluate the different, but concurrent, impacts on eulachons climate, habitat, bycatch and not allow any one explanation to be used as an excuse to overlook possible impacts of the other. References Anonymous Status report: Columbia River fish runs and fisheries, Oregon Department of Fish and Wildlife and Washington State Department of Fisheries, 257 pp. Boutillier, J.A., W.R. Harling, and D.E. Young F.V. SHARLENE K shrimp survey 89-S-1, west coast of Vancouver Island, May 10-16, Can. Data Rep. Fish. Aquat. Sci. 807, 83 pp. Boutillier, J.A., A.N. Yates, and T.H. Butler G.B. REED shrimp cruise , May 3-14, Fish. Mar. Serv. Data Rep. 37, 42 pp. DeLacy, A.C., and B.S. Batts Possible population heterogeneity in the Columbia River smelt. Fisheries Research Institute, College of Fisheries, University of Washington, Circular 198. Hart, J.L Pacific fishes of Canada. Bull. Fish. Res. Board Can. 180, 740 pp.

74 530 Hay et al. Eulachon as an Indicator Species in the North Pacific Hart, J.L., and J.L. McHugh The smelts (Osmeridae) of British Columbia. Bull. Fish. Res. Board Can. 64, 27 pp. Kuhnlein, H.V., A.C. Chan, J.N. Thompson, and S. Nakai Ooligan grease: A nutritious fat used by Native people of coastal British Columbia. J. Ethnobiol. 2: Langer, O.E., B.G. Shepherd, and P.R. Vroom Biology of the Nass River eulachon Canada Department of Fisheries and Environment Tech. Rep. PAC/T-77-10, 56 pp. McAllister, D.E A revision of the smelt family, Osmeridae. Natl. Mus. Can. Bull. 191, 53 pp. Ricker, W.E., D.F. Manzer, and E.A. Neave The Fraser River eulachon fishery, Fish. Res. Board Can. Manuscr. Rep. Biol. Sta. 583, 35 pp. Samis, S.C Sampling eulachon eggs in the Fraser River using a submersible pump. Canada Department of Fisheries and Environment Tech. Rep. PAC/T , 10 pp. Smith, W.E., and R.W. Saalfeld Studies on Columbia River smelt, Thaleichthys pacificus (Richardson). Wash. Dep. Fish. Fish. Res. Pap. 1:3-26. Stewart, The seasonal availability of fish species used by the coast Tsimshians of northern British Columbia. Syesis 8: Ware, D.M., and G.A. McFarlane Fisheries production domains in the northeast Pacific Ocean. In: R.J. Beamish and G.A. McFarlane (eds.), Effects of ocean variability on recruitment and an evaluation of parameters used in stock assessment models. Can. Spec. Publ. Fish. Aquat. Sci. 108:

75 Proceedings Forage Fishes in Marine Ecosystems 531 Alaska Sea Grant College Program AK-SG-97-01, 1997 Declines of Forage Species in the Gulf of Alaska, , as an Indicator of Regime Shift Paul J. Anderson National Marine Fisheries Service, Alaska Fisheries Science Center, Kodiak, Alaska James E. Blackburn Alaska Department of Fish and Game, Kodiak, Alaska B. Alan Johnson National Marine Fisheries Service, Alaska Fisheries Science Center, Kodiak, Alaska Abstract Twenty-four years ( ) of shrimp trawl survey catch data were analyzed in order to reveal changes in the species composition of demersal biomass in the Gulf of Alaska. A shrimp-dominated crustacean species community (mostly Pandalus goniurus and P. borealis) came to an end in the late 1970s and has not yet regained its former level of biomass. Changes in community structure continued with the decline of capelin (Mallotus villosus) in the late 1970s, followed by a buildup of gadid fishes in and pleuronectid fishes in 1984 to the present. Overall, the biomass index, as represented by shrimp sampling trawl, has declined to less than one-half of its former size under the recent fish-dominated environment. This epibenthic regime shift was accompanied by a rapid increase in water temperature which may largely be responsible for the observed abrupt temporal change in species composition. Introduction Simultaneous and abrupt declines of crustacean and fish populations, most notably shrimps of the genus Pandalus and smelts (family Osmeridae), have occurred in the Gulf of Alaska along with increases in densities of gadid fishes and many species of pleuronectid flatfishes.

76 532 Anderson et al. Forage Species Declines Indicate Regime Shift These concurrent changes in several species suggest that they are causally connected in affecting commercial (Anderson 1991) and noncommercial species (Piatt and Anderson 1996) alike, and thus represent a regime shift (Steele 1996). Implicit in the concept of a regime shift is that changes occur throughout the ecosystem and a new community structure is formed. A crustacean and forage fish epibenthic community changed to the current regime dominated by fishes during a brief time period between 1978 and 1981 in the central and western Gulf of Alaska. This shift is well documented by results from a long-term smallmesh trawl survey series conducted before and after the shift (Piatt and Anderson 1996). This paper describes the results from these surveys and presents hypotheses for the observed regime shift. Methods Data used in this study were collected during small-mesh trawl surveys which targeted shrimp as their primary species. The data set is a compilation of nearly 10,000 trawl samples by the National Marine Fisheries Service and the Alaska Department of Fish and Game. Most of the sampling was done with a small-mesh net with 32-mm stretched mesh throughout (Anderson 1991). Survey tows were conducted during daylight in water deeper than 50 m since preliminary surveys had shown low shrimp densities in shallow water (Anderson 1991). Most tows covered an average length of 1-2 km. Survey catches were sorted by species and all species were weighed separately. Occasionally, catches were so large that sub-sampling of the catch was employed after the method described by Hughes (1976). Subsamples were counted to obtain the average weight of individuals. All shrimp and juvenile fish (mostly Pleuronectidae) were combined, weighed, and subsampled for species composition. The subsampled species groups were then counted and weighed to the nearest gram using a triple-beam scale. The extrapolated juvenile weights of each species were added to those of the adults of the same species. Organism counts and weights were converted to density values expressed as either number or kilograms caught per kilometer towed by the sampling gear (catch per unit of effort [CPUE]). Converting density values in this way minimizes possible bias associated with sampling tows of unequal distance or duration. Abundance comparisons for species among years and areas all use CPUE rather than actual catch values. Sampled locations were mapped using the computer program ARCINFO, and data distribution was outlined graphically to define the sampled area over the time series. Species density by area was determined by combining CPUE values for each area by year and computing the mean. Eight bays were chosen for detailed study (Figure 1), representing a broad coverage of the Gulf of Alaska inshore bay ecosystem.

77 Forage Fishes in Marine Ecosystems 533 Figure 1. Location of bays and nearshore sampling sites for small-mesh trawl surveys, Note: Chignik-Castle is a group of three bays: Chignik, Kujulik, and Castle bays. We abstracted major components from the total biomass in order to simplify our analysis for density trends. Two groups of forage species, including shrimps, mainly Pandalus spp., and smelts (Osmeridae), mostly capelin (Mallotus villosus), to a lesser extent eulachon (Thaleichthys pacificus), and small amounts of other smelts, composed the forage species complex. We considered the smelts and shrimps as belonging to the same trophospecies (species group that shares similar prey and predators). Flatfishes (Pleuronectidae) were treated as a group and included five species: arrowtooth flounder (Atheresthes stomias), flathead sole (Hippoglossoides elassodon), yellowfin sole (Pleuronectes asper), rock sole (Pleuronectes bilineatus), and Pacific halibut (Hippoglossus stenolepis). Gadid fishes included Pacific cod (Gadus macrocephalus) and walleye pollock (Theragra chalcogramma). All other species, which made up the remainder of the catch biomass, were treated as a combined element for this study.

78 534 Anderson et al. Forage Species Declines Indicate Regime Shift Results Combined biomass of all species declined in seven of the eight study areas to the lowest CPUE during the period. One area, Two- Headed Island gully, showed low total biomass during the early period. Since most of the data for this period had to be discarded due to incomplete catch sorting, we feel that the low total biomass for this period distorts the results. If this data point is discarded, then the trend of low overall abundance of all organisms fits the same pattern observed for the other areas (Table 1). All areas sampled showed an increase in total biomass as measured by our sampling gear in the latest period ( ). In order to remove fluctuations associated with seasonal onshore and offshore movements of biomass components, we selected catch data from the August-November period to study changes in total biomass. Anderson (1991) hypothesized that shrimp density was most stable at this time of year because of mating aggregations. Ketchen (1961) indicated that inshore cod populations were probably more predominant in the summer and fall because of warmer temperatures before winter cooling. Highest total biomass was kg/km (mean CPUE n = 873, SD = 470.2) during , before declining to kg/km (mean CPUE n = 342, SD = 158.3) in Based on the recent sampling period total biomass has recovered to kg/km (mean CPUE n = 215, SD = 229.3) (Figure 2). The two main forage species groups, shrimps and osmerids, declined from relatively high levels of abundance in to uniformly low abundance during Three areas, Chiniak, Pavlof, and Ugak bays, all showed high levels of osmerids and shrimp simultaneously. In two areas, Pavlof and Chiniak bays, high forage species abundance was coincident with high total biomass. Chignik Bay showed highest osmerid abundance earlier than observed maximum shrimp abundance (Table 1). In the osmerid group, capelin alone composed 84% of total group biomass prior to 1981 and declined thereafter leaving eulachon the major species in the group. Capelin maximum mean CPUE for late summer and fall surveys was in 1972 at 23.7 kg/km; other peaks in abundance occurred in 1976 at 21.2 kg/km and again in 1980 at 15.9 kg/km. Abundance of capelin has remained at less than 0.1 kg/km since 1987 and shows no sign of recovery (Figure 3). Results indicate a close relationship between high total biomass and high forage species abundance. In contrast, low total biomass is related to both low abundance of forage species and high levels of flatfish abundance (Table 1). In order to explore these observed relationships, we used a slug trace plot (Ramsey 1988) to illustrate periods of biomass regime shift for our study areas. This technique uses bivariate time plots of the studied species groups in two dimensions accompa-

79 Forage Fishes in Marine Ecosystems 535 nied by a univariate scatter plot. The relationship between the two forage species is shown in Figure 4. The arrow line on the corresponding plots signals the regime shift observed in the survey data. It is clear from these plots that the relationship of shrimp and osmerid abundance changed between 1976 and 1983, signaling the shift to a new community structure. Discussion A major shift in the physical regime of the Gulf of Alaska occurred in (Royer 1989, Kerr 1992, Trenberth and Hurrell 1995) and is reflected in the shift in species composition data from trawl surveys of inshore bays over a broad region observed in this study (Figure 5). Other studies have shown increased landings of Pacific salmon (Beamish and Bouillon 1993), possibly due to enhanced ocean survival which may be the direct result of increased zooplankton abundance (Brodeur and Ware 1992) or more favorable temperature. Kodiak Island nearshore (10.7 m) water temperature in March averaged 0.48 to 2.01 C during , C during , and C during (Pers. comm., S.F. Blau). Increases in nearshore water column temperature may affect productivity for shrimp and forage fish in a negative way. Aquatic communities integrate the totality of environmental factors that they are exposed to. Our contention is that the physical regime shift co-occurred with the shift from the crustacean and forage fish regime to the current epibenthic community now dominated by cod, pollock, and pleuronectid flatfishes, and was the primary cause of the epibenthic community shift. Shrimp declined uniformly throughout all study areas, but one species (Pandalus goniurus) that was formerly a significant part of the shrimp biomass became nearly extinct (Figure 6) while the other primary species (P. borealis) declined, but not to levels of near-extinction. This observed change demonstrates that some species are more vulnerable to being extinguished from the nearshore ecosystem as a result of regime shift. This species was not heavily targeted by commercial shrimpers, and declines after closure of commercial fisheries continued. We hypothesize that the near-extinction of P. goniurus was caused by sustained higher winter temperatures that took place in the late 1970s (Royer 1989). This species is found in shallower waters than P. borealis and these areas are subject to high residual winter cooling. These distribution traits along with abrupt changes in winter temperatures may explain the region-wide regime shift. Influxes of Pacific cod into the inshore bays and gullies where dense shrimp and osmerid populations occurred was a destabilizing factor on those populations and was partially responsible for the observed ecosystem regime shift in the Gulf of Alaska. Cod were virtually absent in

80 536 Anderson et al. Forage Species Declines Indicate Regime Shift Table 1. Mean catch in kilograms per kilometer trawled of selected species groups by study area and selected periods. Period Total Shrimps Osmerids Pleuronectids Gadids Alitak Bay ns ns ns ns Chignik Bay Chiniak Bay ns ns ns ns ns Kiliuda Bay ns Marmot Bay ns ns ns ns Pavlof Bay ns = not sampled

81 Forage Fishes in Marine Ecosystems 537 Table 1. (Cont d.) Period Total Shrimps Osmerids Pleuronectids Gadids Two-Headed Ugak Bay ns ns ns ns ns ns ns ns ns ns = not sampled. Figure 2. Mean CPUE (expressed as kilograms caught per kilometer trawled) of total biomass for August-November, , in all eight sampling sites combined.

82 538 Anderson et al. Forage Species Declines Indicate Regime Shift Figure 3. Mean CPUE of capelin from August-November trawl surveys, , in all sampling locations combined.

83 Forage Fishes in Marine Ecosystems 539 Figure 4. Slug traces of shrimps and osmerids from several bays; regime shift identified by arrow line on scatterplots. (Please note difference in scales of mean CPUE for species groups in bivariate time plots.)

84 540 Anderson et al. Forage Species Declines Indicate Regime Shift Figure 5. Species composition represented by proportional contribution in August-November total biomass in all sampling sites combined.

85 Forage Fishes in Marine Ecosystems 541 Figure 6. Mean CPUE of Pandalus borealis and P. goniurus from all sampling areas,

86 542 Anderson et al. Forage Species Declines Indicate Regime Shift inshore bays during the early 1970s (Albers and Anderson 1985) (Figure 5). We believe that warming water column temperatures may allow cod to remain in our study areas throughout the winter instead of migrating offshore when temperatures are cooler (Ketchen 1961). This increased contact with the forage base probably contributed further to the observed decline of shrimps and osmerids that continued well after the end of most inshore shrimp trawl fisheries in the late 1970s (Albers and Anderson 1985). In conclusion, our analysis shows a marked decline in the available biomass after the shift from the crustacean regime to the regime dominated by fishes (Figures 2 and 5). The declines in epibenthic biomass, as observed in this study, were opposite of the increase in landings and abundance of many species of Pacific salmon (Beamish and Bouillon 1993). A change in the higher trophic levels and composition of zooplankton was also coincident with the regime shift (Brodeur and Ware 1992). Since many forage species, including capelin and shrimp, are planktivores, this observed change in plankton composition could explain the uniform decline of these species. Abrupt changes in the physical regime with concurrent or slightly delayed reaction from the epibenthic ecosystem had an extreme effect on the inshore fishing fleet and processing industry in the central and western Gulf of Alaska. The regime shift, as described in this paper, occurred rapidly and may shift again from a fish-dominated to another community regime. These species composition shifts are preceded by changes in the physical environment. Monitoring water column temperature and changes in the epibenthic organisms in many areas of the Gulf of Alaska could be used to forecast future changes and perhaps lead to less disruption in the fishing industry when these regime shifts occur. Acknowledgments This project was partially supported by the Alaska Predator Ecosystem Experiment (APEX) which was funded by a grant from the Exxon Valdez Oil Spill Trustee Council. We thank Tamara Olson (Natural Resource Research and Consulting) for conducting the GIS analysis. Finally, we thank the crew and scientists from the Alaska Department of Fish and Game and the National Marine Fisheries Service who spent many months at sea collecting the data for our analysis. References Albers, W.D., and P.J. Anderson Diet of the Pacific cod, Gadus macrocephalus, and predation on the northern pink shrimp, Pandalus borealis, in Pavlof Bay, Alaska. U.S. Natl. Mar. Fish. Serv. Fish. Bull. 83:

87 Forage Fishes in Marine Ecosystems 543 Anderson, P.J Age, growth, and mortality of the northern shrimp Pandalus borealis Kröyer in Pavlof Bay, Alaska. U.S. Natl. Mar. Fish. Serv. Fish. Bull. 89: Beamish, R.J., and D.R. Bouillon Pacific salmon production trends in relation to climate. Can. J. Fish. Aquat. Sci. 50: Brodeur, R.D., and D.M. Ware Long-term variability in the zooplankton biomass in the subarctic Pacific Ocean. Fish. Oceanogr. 1: Hughes, S.E System for sampling large trawl catches of research vessels. J. Fish. Res. Board Can. 33: Kerr, R.A Unmasking a shifty climate system. Science (Washington, D.C.)255: Ketchen, K.S Observations on the ecology of the Pacific cod (Gadus macrocephalus) in Canadian waters. J. Fish. Res. Board Can. 18: Piatt, J.F., and P. Anderson Response of Common Murres to the Exxon Valdez oil spill and long-term changes in the Gulf of Alaska marine ecosystem. In: S.D. Rice, R.B. Spies, D.A. Wolfe, and B.A. Wright (eds.), Exxon Valdez Oil Spill Symposium Proceedings. American Fisheries Symposium No. 18: Ramsey, F.L The slug trace. American Statistician 42:290. Royer, T.C Upper ocean temperature variability in the northeastern Pacific Ocean: Is it an indicator of global warming? J. Geophys. Res. 98: Steele, J.H Regime shifts in fisheries management. Fish. Res. 25: Trenberth, K.E., and J.W. Hurrell Decadal coupled atmosphere-ocean variations in the North Pacific Ocean. In: R.J. Beamish (ed.), Climate change and northern fish populations. Can. Spec. Publ. Fish. Aquat. Sci. 121:15-24.

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89 Proceedings Forage Fishes in Marine Ecosystems 545 Alaska Sea Grant College Program AK-SG-97-01, 1997 Global Climate Cycles and Pacific Forage Fish Stock Fluctuations Leonid B. Klyashtorin Institute of Fisheries and Oceanography (VNIRO), Moscow, Russia Abstract Strongly smoothed global and Northern Hemisphere surface air temperature anomaly (dt ) and Aleutian low pressure index (ALPI) trends demonstrate the general direction of global climate changes, although without reliable prognostic meaning for Pacific fish production. The atmospheric circulation index (ACI) trend characterizing the principal direction of air mass transport in the Northern Hemisphere is in phase with the general trends in the global dt index and global geophysics characteristic: the earth rotation velocity index (ERVI). The ACI and ERVI trends correlate closely with the main Pacific commercial stock trends: Peruvian, Japanese, and California sardines, anchovy, Pacific salmon, Alaska pollock, Chilean jack mackerel, Pacific cod, tunas, and some others. It is possible to consider ACI and ERVI as a prognostic index and to forecast the dynamics of main commercial stocks for 2-15 years based on a climatic regime model. Variation in the harvest of Pacific commercial species over the last century can be pictured as two sequential natural climate-governed production cycles with maxima in the late 1930s and late 1980s-early 1990s. The recent cycle is not yet complete, but is coming to the phase similar to the climatic phase of the 1940s and 1950s. The evolution of the new climatic phase will have serious ecological consequences not only for oceanic but also for terrestrial biota of the Pacific Rim region. Introduction The impacts of large-scale climate change on the fish productivity of the oceans is an important scientific and economic problem. The simultaneous fluctuations of sardine (and anchovy) stocks in the North and South Pacific indicate they are governed by global climate events (Lluch- Belda et al. 1989, Kawasaki 1992a, Klyashtorin and Sidorenkov 1996). The mechanisms which initiate, sustain, and terminate such outbursts

90 546 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations are not clear. Reliable correlation linkages between long-term stock fluctuations and global climate characteristics also are not known. The main purposes of this paper are follows: (1) to ascertain the main Pacific forage and pelagic fish stocks involved in the long-term fluctuations; (2) to reveal climate characteristics reliably correlated with long-term commercial stock dynamics; and (3) to display global climate indices which could make it possible to forecast large-scale pelagic fish stock fluctuations in the Pacific Ocean. Materials and Methods Commercial statistics for the Pacific region are available only for years since the 1920s. The main sources of statistical data were: FAO Yearbook of Statistics for , Pacific salmon catches for (VNIRO 1989), Kawasaki (1992b, Klyashtorin and Smirnov (1992), and Shuntov et al. (1993). Catch alone is acknowledged to be a crude measure of abundance. However, the changes in catches of main commercial species are so marked there can be little doubt that they reflect real changes in population size (Lluch-Belda et al. 1989). Global and Northern Hemisphere surface air and sea temperature anomaly (dt ) data are from Halpert et al. (1994). The Aleutian low pressure index (ALPI) is used as an index of historical weather over the North Pacific Ocean. The ALPI was calculated as the area (square kilometers) of the North Pacific Ocean covered by Aleutian low pressure system less than kpa. Annual values of ALPI since 1900 are from Beamish and Bouillon (1993). The atmospheric circulation index (ACI) was measured in the Atlantic- European region by the G. Wangengeim method. The ACI time series has been kept continually since 1891 (Girs 1974). According to this method, all observable forms of atmospheric circulation are divided into two main types by the direction of air mass transport : zonal (latitudinal) or meridional ones. The ACI values used in this paper are the zonal (West + East) form of air mass transport. The ACI time series are presented as integrated anomalies curve of The materials were provided by the Russian Federation Arctic and Antarctic Institute (St. Petersburg). The annual earth rotation velocity index (ERVI) data expressed as dimensionless values are from Sidorenkov and Svirenko (1991). Results The trends of dt and ALPI presented (Figure 1) are highly variable and only 13-year smoothing reaches the level of statistical significance by the F criterion. In contrast, ACI variability is substantially less. The ACI trend and smoothed dt and ALPI trends had a similar shape: maximum in the 1930s and minimum in the 1950s and 1960s, with a new maximum in the 1980s and 1990s.

91 Forage Fishes in Marine Ecosystems 547 Catch dynamics for Japanese sardine, California sardine, and the species of Pacific salmon (Figure 2) have similar shapes with maxima in the late 1930s, depression in the 1950s and 1960s, and recent maxima in the late 1980s. The ACI curve shows good accordance with catch dynamics during the twentieth century. The similar shape of ACI and catch trends was observed for main commercial species in the South Pacific (Figure 3) such as Chilean jack mackerel and Peruvian sardine. The Peruvian anchovy catch curve is roughly out of phase as regards the ACI curve. Pacific fishery statistics mainly cover the second half of the century. For adequate evaluation of relationships between climatic characteristics and commercial catch dynamics it is expedient to treat each half of the century separately. Preliminary analysis shows that unsmoothed ALPI and dt trends are weakly correlated with commercial catch trends. The climatic index most closely correlated with long-term fluctuations of main commercial stocks is the ACI. Analysis of the relationship between the ACI and catches for the first and second halves of the century (Figure 4) shows the following. Correlation coefficients for Japanese sardine were ; California sardine, ; and Pacific salmon, The curves for the Pacific salmon catch have a saw-like form because of the nature of pink salmon stock dynamics: odd and even year fluctuations. After 5-year smoothing the correlation coefficient for the salmon catch curve increases to High correlations between catches and ACI (Figure 5) were observed for for Northern Hemisphere Alaska pollock (0.77) and Pacific cod (0.84). South Pacific catches for (Figure 5) were tightly correlated with the ACI. The correlation coefficient for Peruvian sardine was 0.95, and for Chilean jack mackerel, The correlation coefficient between ACI and anchovy catch was 0.39 (Figure 6). This gives us a possibility to suppose (as a first approximation) the out-of-phase character of dynamics in sardine and anchovy stocks. The total Pacific catch for (Figure 7) was closely correlated with the ACI (correlation coefficient = 0.93). A high correlation between ACI and catch was found for four major commercial species: Japanese and Peruvian sardines, Alaska pollock, and Chilean jack mackerel (excluding anchovy) = 0.98; and tunas and tuna-like species = Discussion and Conclusions Apart from the oscillations of sardine and anchovy stocks in the subtropics, a number of highly abundant pelagic species Pacific salmon, Alaska pollock, Chilean jack mackerel, Pacific cod, Pacific tunas, and some others are involved in long-term climate-governed fluctuations in all climatic zones of the Pacific from the Arctic to the tropics

92 548 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations Figure 1. Trends in the air surface temperature anomalies in the Northern Hemisphere (A), Aleutian low pressure index (B), and atmospheric circulation index (C) for Figure 2. Major commercial species catches in the North Pacific and atmospheric circulation index, (all curves unsmoothed).

93 Forage Fishes in Marine Ecosystems 549 Figure 3. Major commercial species catches in the South Pacific and atmospheric circulation index, (all curves unsmoothed).

94 550 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations Figure 4. Relationship between major commercial species catches and atmospheric circulation index in the North Pacific for (A, B, C) and (D, E, F) (R, correlation coefficient; N = 62, P <0.001 for all comparisons).

95 Forage Fishes in Marine Ecosystems 551 Figure 5. Relationship between major commercial species catches and atmospheric circulation index in the North Pacific (A, B) and South Pacific (C, D) for (R, correlation coefficient; N = 48, P <0.001 for all comparisons).

96 552 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations Figure 6. Relationship between Peruvian anchovy catch and atmospheric circulation index, (R, correlation coefficient; N = 66, P <0.05). Figure 7. Relationship between Pacific commercial species catches and atmospheric circulation index, : A, total Pacific marine fish catch; B, total for four major commercial species (Japanese and Peruvian sardine, Alaska pollock, and Chilean jack mackerel, excluding anchovy); C, total for tunas, bonitos, and billifishes (R, correlation coefficient; N = 48, P <0.001 for all comparisons).

97 Forage Fishes in Marine Ecosystems 553 Figure 8. Atmospheric circulation index and earth rotation velocity index, Figure 9. Atmospheric circulation index, earth rotation velocity index, and periods of Japanese sardine stock bursts according to Japanese historical documents for

98 554 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations Figure 10. General trends in climatic indices and commercial catches in the Pacific for (A) and (B); dt and ALPI smoothed by 13- year averaging, and ACI, ERVI, and all catch trends smoothed by 5- year averaging. The data for each curve are expressed as percentages of maximum value. The arrows indicate curve maxima.

99 Forage Fishes in Marine Ecosystems 555 (Klyashtorin and Smirnov 1995). This list can be supplemented with herring, which like anchovy exhibit out-of-phase stock fluctuations in relation to sardine (Kawasaki 1992b). The total catch of these species reaches up to 45% of the total Pacific marine fish harvest. Peruvian anchovy stock dynamics are roughly out of phase in relation to the ACI and sardine catch curves. Similar trends were observed for Japanese and California anchovies and Pacific herring (Kawasaki 1994). The sardine-anchovy and sardine-herring stock fluctuations are likely to be a climate-triggered process (Kawasaki 1992b). The ACI was recorded in the Atlantic-European region. Therefore, its close correlation with Pacific pelagic catch trends seems at first sight to be a paradox. However, ACI trends are in phase with the smoothed curves of the global and Northern Hemisphere temperature anomalies and ALPI. The ACI curves likely reflect the change of long-term atmospheric circulation on the global scale (Girs 1974). This is confirmed by a strong correlation between ACI and ERVI (Figure 8). A hypothetical functional relationship between ACI and ERVI was suggested by Sidorenkov and Svirenko (1991). The periodicity of Japanese sardine stock bursts is about 60 years for the last 400 years (Kawasaki 1994). A good correspondence in phases between trends of ACI, ERVI, and periods of Japanese sardine outbursts has been recorded since the 1800s (Figure 9). This 60-year type of cycle is confirmed by data on reconstruction of California sardine and anchovy stock variations over the past two millennia (Baumgartner et al. 1992). The notion of roughly 60-year cycles of fish productivity is supported by recent data on low-frequency global climate variability (Ware and Thomson 1991, Kawasaki 1994, Schlesinger and Ramankutty 1994, Ware 1995). Long-term fluctuations of pelagic fish stocks in the Pacific over the twentieth century can be presented as the passing of two natural climatic-production cycles (Figure 10). The first cycle developed in the early decades of the century with maximum production in the late 1930s and the second developed from the early 1970s, with maximum production in the late 1980s and early 1990s. The final (descending) phase of the second cycle is coming, similar to the 1940s and 1950s. The behavior of all climatic index trends dt, ALPI, ACI, and ERVI is similar to that observed for the 1940s and 1950s. The close correlation between abundance of major pelagic species and climatic and geophysical characteristics makes it possible to consider trends in pelagic fish catches as a sensitive indicator of climate change. In many instances biological organisms are integrators of environmental variables and may be more sensitive to low frequency climate events than physical time series (Polovina et al. 1994). Mechanisms of climate impacts on productivity in marine ecosystems are not clear. Apparently, the main causative events may be large-

100 556 Klyashtorin Global Climate Cycles and Fish Stock Fluctuations scale change in atmospheric and water mass transport (Bakun 1990, Hsien and Boer 1992, Kawasaki 1992b). The ACI and ERVI can be considered as long-term forecasting indices which give us an opportunity to predict the dynamics of major pelagic species stocks for the next 2 to 15 years. The Pacific region is coming into the final phase of the second longterm climatic cycle. The evolution of this phase will have serious consequences not only for oceanic, but for terrestrial biota of the Pacific Rim region as well. References Bakun, A Global climate change and intensification of coastal ocean upwelling. Science 247: Baumgartner, T.R., A. Soutar, and V. Ferreira-Bartrina Reconstruction of the history of Pacific sardine and northern Pacific anchovy populations over the past two millennia from sediments of the Santa Barbara basin. CalCOFI Rep. 33: Beamish, R.J., and D.R. Bouillon Pacific salmon production trends in relation to climate. Can. J. Fish. Aquat. Sci. 50: FAO (Food and Agriculture Organization of the United Nations) Yearbook of Fishery Statistics FAO Fish. Ser Girs, A.A Macrocirculation method for long-term meteorological prognosis. Hydrometizdat Publ., Leningrad. 480 pp. (In Russian.) Halpert M., G. Bell, V. Kousky, and C. Roplevski (eds.) Fifth annual climate assessment U.S. Department of Commerce, NOAA, Climate Analysis Center. 110 pp. Hsien, W.W., and G.I. Boer Global climate change and ocean upwelling. Fish. Oceanogr. 1: Kawasaki, T. 1992a. Climate-dependent fluctuations in Far Eastern sardine population and their impacts on fisheries and society. In: M. Glantz (ed.), Climate variability, climate change, and fisheries. Cambridge University Press, pp Kawasaki, T. 1992b. Mechanisms governing fluctuations in pelagic fish populations. In: Benguela trophic functioning. S. Afr. J. Mar. Sci. 12: Kawasaki, T Recovery and collapse of the Far Eastern sardine. Fish. Oceanogr. 2: Kawasaki, T A decade of the regime shift of small pelagics from the FAO expert consultation (1983) to the PICES III (1994). Bull. Jpn. Soc. Fish. Oceanogr. 58(4): Klyashtorin, L., and N. Sidorenkov Long-term climatic change and pelagic fish stock fluctuations in the Pacific. Izv. Pacific Research Center of Fisheries (TINRO-CENTRE) 119: (In Russian with English summary.)

101 Forage Fishes in Marine Ecosystems 557 Klyashtorin, L., and B. Smirnov North Pacific salmon stock dynamics and some aspects of salmon ranching. ECINAS (In Russian. Russian Federation Committee of Fisheries), Moscow, Aquaculture Ser. 2:1-36. Klyashtorin, L., and B. Smirnov Climate-dependent salmon and sardine stock fluctuations in the North Pacific. Can. Spec. Publ. Fish. Aquat. Sci. 121: Lluch-Belda, D., R. Crawford, T. Kawasaki, A. MacCall, R. Parrish, R. Shwartzlose, and P. Smith World-wide fluctuations of sardine and anchovy stocks. The regime problem. S. Afr. J. Mar. Sci. 8: Lluch-Belda, D., R. Shwartzlose, R. Serra, R. Parrish, T. Kawasaki, D. Hedgecock, and R. Crawford Sardine and anchovy regime fluctuations of abundance in four regions of the world ocean: A workshop report. Fish. Oceanogr. 2: VNIRO Pacific salmon commercial catch, Statistical collected volume. VNIRO, Moscow. 213 pp. (In Russian.) Polovina, J.J., G.T. Mitchum, N.E. Graham, M.P. Craig, E.E. Demartini, and E.E. Flint Physical and biological consequences of a climate event in the central North Pacific. Fish. Oceanogr. 3:5-21. Schlesinger, M.E., and N. Ramankutty An oscillation in the global climate system of period years. Nature 367: Shuntov, V., A. Volkov, O. Temnych, and E. Dulepova Alaska pollock in the ecosystems of Far Eastern seas. Pacific Institute of Fisheries and Oceanography, Vladivostok. 426 pp. (In Russian.) Sidorenkov, N., and P. Svirenko Diagnosis of some parameters of global water change based on the data of irregularity of the earth rotation velocity. Proc. Acad. Sci. Geogr. Ser. 11(5):6-23. (In Russian.) Sidorenkov, N., and P. Svirenko Multiannual atmospheric circulation change and climate oscillation in first synoptical region. Proceedings of Hydrometcenter 316: (In Russian.) Ware, D.M A century and a half of change in the climate of the northeastern Pacific. Fish. Oceanogr. 4: Ware, D.M., and R.E. Thomson Link between long-term variability and fish production in the northeast Pacific Ocean. Can. J. Fish. Aquat. Sci. 48:

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103 Proceedings Forage Fishes in Marine Ecosystems 559 Alaska Sea Grant College Program AK-SG-97-01, 1997 Continental Shelf Area and Distribution, Abundance, and Habitat of Herring in the North Pacific D.E. Hay and P.B. McCarter Department of Fisheries and Oceans, Pacific Biological Station, Nanaimo, British Columbia, Canada Abstract Pacific herring (Clupea pallasi) life history is closely associated with the continental shelf and adjacent coastal areas. In general, throughout the Northern Hemisphere, areas with large herring populations have broad continental shelves, and areas with small populations have small or narrow shelves. Based on our own observations and data, we suggest that adult Pacific herring distribution is confined mainly to water with depths not exceeding 200 m. Within this depth range, herring aggregations often associate closely with the bottom in daylight hours, rising in darker hours. We do not often see acoustic targets resembling herring or catch herring in deeper water. We observe that summer distributions, when herring feed extensively, seem to be more diffuse than winter so the available areas for summer feeding may be part of the fixed carrying capacity for herring in all areas. This paper presents maximal estimated stock sizes for 14 different Pacific and Atlantic herring stocks, or production areas, and compares this with estimates of the associated shelf area. As an approximation, the density-independent maximal biomass of each stock is defined mainly by the availability of shelf area. We suggest this is a rough approximation of summer feeding habitat, and the maximal average density seems to be about 10 g/m 2. Pacific herring life history, however, includes at least five different stages (egg, larval, juvenile, adult summer habitat, adult winter habitat) and each stage might use different habitats. The availability of other habitats may impose limitations to population size that supersede continental shelf area as a limiting habitat. Also, other density-independent factors (i.e., annual variation in oceanographic climate) and density-dependent factors (predation, food availability) often operate within the constraints imposed by habitat limitation.

104 560 Hay & McCarter Herring in the North Pacific Introduction In their pioneering text on animal populations, Andrewartha and Birch (1954) defined an animal s environment as everything that may influence its chance to survive and multiply. They divided the environment into four broad categories: (a) Weather, (b) Food, (c) Other animals and pathogens, (d) a place in which to live. They qualified this list so that food (item b) includes prey species and item (c) includes predator species. For the purposes of the present paper this list of categories is useful, even if the reader does not concur with the definition or the categories. The present paper is concerned mainly with part (d), a place in which to live, and we specifically suggest that the area of the continental shelf is a vital factor affecting herring, as an important forage fish species. The vast scientific literature on herring contains many papers that comment on possible effects of weather or climate on food and predators on herring populations. For instance, the famous Hjort hypothesis (Hjort 1914) and the equally famous match-mismatch hypothesis (Cushing 1972) consider the role of food availability for larval survival, although it is not necessarily clear if densities of larval fish are sufficiently high to limit their food supply (Cushing 1983). There are many studies on the effect of predation as a limiting factor on herring populations (e.g., Walters et al. 1986, Ware and McFarlane 1986). Other studies have examined climate changes or climate-induced changes on predation (Ware and McFarlane 1989, 1995). There are very few examples, however, of studies that comment explicitly on spatial limitations or habitat limitations of herring population size. A possible exception is the well known suggestion of Iles and Sinclair (1982) that the spatial dimensions and hydrographic characteristics of larval retention areas determine maximal population size. At the conclusion of this paper we indicate how our modest suggestion is related to some of these previous influential theories. In this paper we repeat and refine a suggestion made by Hay (1992) that the environment of Pacific herring, and perhaps all herring, is very closely tied to the relatively shallow (<200 m) waters of the continental shelf and that this is a limiting factor of the ultimate size of herring populations. We support this contention by relating the estimated (maximal) sizes of some herring populations to the area of shelf that supports them. We caution that the relationship is only an approximation and probably does not apply to all life history stages of herring. For the purposes of discussion, we distinguish four different herring life history stages that require five distinct habitats, each of which may be limiting in one or more areas. (1) Spawning habitat, in either intertidal or shallow subtidal areas, in sheltered waters may be limited, particularly in Asian waters (Benko et al. 1987) but this is probably not generally the case in most North American waters (Hay and Kronlund 1987). (2) Pelagic larval habitat is mainly near shore (<5 km), with a duration of about 2-3

105 Forage Fishes in Marine Ecosystems 561 months. It is not clear if this habitat is limiting. (3) Juvenile rearing habitat is mainly shallow, near shore (<1 km), and occupied for months. We speculate that habitat may be limiting in the Bering Sea. (4) Adult summer feeding habitat is occupied for about 6-8 months per year and varies widely, from very small coastal inlets to broad areas on the shelf that require extensive, precisely timed migrations. We suggest that this is limiting for much of the southern range of herring in North America south of the Bering Sea. (5) Adult overwintering habitat occupied for 3-4 months usually is associated with nearshore channels ( m), and often is in the general area of spawning areas. We observe that in southern British Columbia these areas vary annually, so many different areas appear to have potential as winter habitat. The continental shelf area, as a population limiting factor, applies only to the summer feeding stage of herring. At all other stages other factors may be limiting, and this may account for much of the variation among populations. In particular, limited juvenile rearing habitat may be a major limiting factor in some populations. Materials and Methods Data on the areas of continental shelves were extracted from published literature as indicated in Table 1. Estimates of herring population sizes also were based on published estimates in the literature. The observation that most Pacific herring are not encountered at depths deeper than 200 m is based on acoustical surveys conducted from 1984 to 1993 (Hay and McCarter 1995). Results and Discussion Shelf areas and herring population sizes The area of the shelf from 0 to 200 m in depth is shown in Figure 1, as the light area adjacent to the coast, for the northeast Pacific from California to the Bering Sea. Although narrow relative to other areas, the coast of British Columbia has one of the widest shelf areas in the Western Hemisphere (excluding the Bering Sea) but the maximal herring population size is only about 400,000 metric tons (and this includes southeastern Alaska). This is not large when compared to the herring biomass of the North Sea, or the Norwegian coast or even the Baltic. In all these areas, these stocks are distributed over about 6-7 degrees of latitude, about the same as the coastline of British Columbia and southeastern Alaska. The list of herring stocks, the area of associated continental shelf, and maximum estimated biomass are shown in Table 1. The estimated herring density is calculated in terms of the quotient of the maximal biomass and the area (g/m 2 or tons/km 2 ). These data indicate that a standing biomass of about 10 g/m 2 is maximal in several different areas (Figure 2). A regression of the population size by the estimated shelf area (Figure 3) is significant (P < 0.01, r 2 = 0.36). The

106 562 Hay & McCarter Herring in the North Pacific Table 1. Comparison of continental shelf area (to a depth of 200 m) and maximum herring biomass in thousands of tons from different herring populations (adapted and modified from Hay 1992). Density Shelf (tons/km 2 Location Biomass area (km 2 ) or g/m 2 ) 1. Sea of Okhotsk 800 a 368 b Eastern Bering Sea (a) ,166 c 687 d 1.7 (b) ~150 e Sea of Japan (Hokkaido stock) 1,000 f North and central California 50 g 25 h Washington (outer coast)/ Oregon 10 i British Columbia/ Southeast Alaska Gulf of Alaska, Prince William Sound 150 k 17 l Newfoundland 490 m Nova Scotia/ Gulf St. Lawrence 348 m New England/Georges Bank 1,140 n Norwegian shelf/coast 10,000 o 1,300 o North Sea 3,300 p Skagerrak/Kattegat 200 q Baltic 3,000 r Estimates from Gulland (1970) unless indicated otherwise. Extensive migrations of Norwegian herring confound estimates for them. a Based on an estimate by Benko et al. (1987). b Table in Kennish (1990). c Estimate based on analysis in Fried and Wespestad (1985). d Gulland (1970). e Approximation based on Fried and Wespestad (1985) and Lebida and Sandstone (1988). f Minimum estimate based on catches which once approximated 1 million t (Morita 1985, Chikuni 1985). g Based on Spratt (1981). h Based on a mean continental shelf width of 25 km (Gulland 1970) by a latitudinal range of 1,000 km. i Estimate by authors including Butler (1980). j Approximate estimate of 300,000 t for B.C. based on Hourston (1980) and a maximum of 71,000 t for southeastern Alaska that had a maximal catch of 71,000 t in 1929 (Reid 1971). k Estimate of 1991 catch plus spawning escapment (Funk and Harris 1992). l Estimate based on approximately 1 2 of the Gulf area from Gulland (1970). m Moores (1980). n Antony and Waring (1980). o Dragesund et al. (1980). Estimates of the shelf area include areas north of the Norwegian coast and may be misleading. p Saville and Bailey (1980). q Estimates by authors based on various communications including ICES manuscript reports. r Anon ICES Working Group estimate.

107 Forage Fishes in Marine Ecosystems 563 Figure 1. The northeast Pacific ocean shelf area between depths of m is shown as the light area adjacent to the coast. This illustrates the narrow continental shelf from California to southeastern Alaska and the wider shelf in western Alaska. Figure 2. Histogram of the herring density estimates, based on the data in Table 2. Maximal densities are approximately 10 g/m 2.