The Bering Sea Ecosystem (1996)

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BIOLOGY OF HIGHER TROPHIC LEVELS 72 4 Biology of Higher Trophic Levels The Bering Sea contains many bird, mammal, and commercially important fish and invertebrate species. The Bering Sea ecosystem can be divided into five major regions: the eastern Bering Sea, the Aleutian Islands, the Gulf of Alaska, the Aleutian Basin, and the western Bering Sea. The state of knowledge and the history of exploitation vary for different regions of the Bering Sea. For some species with relatively good histories of exploitation or protection, statistical data are available that provide information on species distributions and magnitude of variability. Generally, the most information is known about the eastern Bering Sea, Aleutians, and Gulf of Alaska, followed by the Aleutian Basin and then the western Bering Sea. This imbalance in data and knowledge on the five regions and the species themselves makes the study of the Bering Sea ecosystem as a whole very difficult. INVERTEBRATES Life History and Distribution Although there are many benthic and pelagic invertebrates in the Bering Sea, only a few are commercially significant. Because of their commercial importance, the most data are available on the squid, crabs, scallops, and shrimp. Squid (Berryteuthis sp. and Gonatus sp.) Several species of squid inhabit the Bering Sea seasonally and also are widely distributed. The exact nature and size of the resource are poorly understood. Squid populations are thought to be large and mobile and to live at both mid-water and near-surface depths. Spawning for some species may extend from spring to fall; sexual maturity may be reached in two years or less. Fertilization is internal. The number of eggs spawned per individual is low compared to groundfish, and the eggs may be attached to seaweeds or the seafloor. Predators of squid are marine mammals and pelagic fishes. 

BIOLOGY OF HIGHER TROPHIC LEVELS 73 King Crab (Paralithodes spp. and Lithodes sp.) Three species of king crabs are found in the Bering Sea and Aleutian Islands region. The red king crab (P. camtschatica) is the largest, most widespread, and most abundant. They are generally found on the continental shelf in the eastern Bering Sea, Aleutian Islands, and Gulf of Alaska to northern British Columbia, generally at depths of 180 m or less (Hayes, 1983). In the western Bering Sea, two large populations of red king crab have been identified—the first in the Sea of Okhotsk region along its broad continental shelf and the west Kamchatka shelf (Vinogradov, 1970), and the second in the northwest Ayano-Shantarskii (Rodin and Myasoyedov, 1982). In addition, relatively small populations exist along the seacoast, including western Sakhalin, Aniva Bay, Tereniya Bay, and east Kamchatka, and near the southern Kurile Islands (Rodin, 1989). The blue king crab (P. platypus) has a more limited distribution. Bering Sea populations are found around St. Lawrence Island, St. Matthew Island, and the Pribilof Islands. Life history is similar to that of the red king crab, described below, though the blue king crab may only breed only on a biennial basis, with spawning occurring during the spring (Stevens et al., 1993). When in the juvenile stage, it tends to concentrate in rocky and shell hash substrates (Armstrong et al., 1985). The brown, or golden, king crab (L. aequispina) is the smallest of the three commercial species, and it inhabits deep water (> 180 m) along the continental slopes of the North Pacific Ocean and the Bering Sea. Little is known of its life history. Whereas adult red king crab feed offshore and migrate inshore for spawning, juveniles are found in the littoral zone and shallower water. In the Bering Sea, adults prefer bottom temperatures of 0° to 5.5° C, suggesting a temperature influence on distribution. Molting and spawning take place in shallow (10 to 50 m) waters in late winter and early spring. Growth of red king crab is discontinuous at time of molts. The U.S. fishery begins to capture them when they are around eight years old. King crab are bottom-foraging omnivores. Principal food sources includes starfish, clams, other mollusks, small crabs, shrimps, other crustaceans, worms, fish, and algae. Predators of king crab include yellowfin sole, Pacific cod, walleye pollock, and Pacific halibut (Wooster, 1992). Females can carry up to 200,000 eggs for a year in the brood pouch before they hatch. Larvae molt four times in a pelagic phase and then settle to the seafloor. Juveniles move into shallow waters to create dense pods ranging from thousands to hundreds of thousands of individuals. King crabs reach maturity at four or five years of age and breed annually (Gusey, 1979). Trawl surveys provide the longest limited information on interannual variation among king and Tanner crab stock units; fishery scientists have conducted independent stock assessments and surveys. Regular systematic trawl surveys for king crab began in the eastern Bering Sea in 1955 and, except for a hiatus from 1962 to 1966, have continued to date. Beginning in 1971, the station pattern of the trawl survey was expanded to include the full range of eastern Bering Sea crabs. Also in 1971, a pot survey for king crab was initiated in the Kodiak region of the Gulf of Alaska. The data from these surveys provide the longest and most consistent time series of survey data available to measure fluctuations in North Pacific crabs. The results of these surveys and comparisons with commercial catch statistics are given in 

BIOLOGY OF HIGHER TROPHIC LEVELS 74 Figures 4.1 (eastern Bering Sea; Hayes, 1983; R.S. Otto, personal communication) and 4.2 (Kodiak; Hayes, 1983). Hayes (1983) concluded that interannual variations in abundance of the exploitable portion of king crab stocks have ranged over an order of magnitude in both the eastern Bering Sea and Kodiak. These fluctuations result from the occurrence of particularly successful cohorts that can be observed to grow and progress through successive sample years, indicating that the sources of these variations operates early in the crab's life history. Similar patterns can be seen for eastern Bering Sea Tanner crab and snow crab. Wooster (1992) chronicled the sporadic fluctuations of king crab over the last three decades. Combining his data (Figure 4.3) with those already shown, patterns in crab dynamics emerge. Red king crab biomass seems to grow quickly, owing to a small number of strong cohorts, and decline quickly as the cohorts either die or are fished out. This happened in Kodiak (central areas in Figure 4.3) in the late 1960s and early 1980s and in the Bering Sea (Figure 4.1) in the late 1950s, late 1970s, and early 1980s. Tanner Crab (Chionoecetes spp.) Tanner crabs are found throughout the Bering Sea region. Two species are relatively large and therefore are of commercial importance. The Tanner crab C. bairdi is the larger of the two species and is usually encountered in the same habitat as red king crab. The snow crab C. opilio is smaller but believed to be the most abundant of the Tanner crabs. It is found in the northern and central Bering Sea on the continental shelf of Russia and Alaska (Slizkin 1989). Eastern Bering Sea Tanner crab (and snow crab) exploitable biomasses peaked in the mid-1970s and again in the late 1980s and early 1990s. The food and feeding habits of Tanner crab are similar to those of king crab; in the larval phase they feed on plankton, in the juvenile phase on benthic diatoms, hydroids, and detritus, and in the adult phase on such benthic organisms as crustaceans, bivalves, brittle stars, echinoids, worms, fish and gastropods. They are eaten by eelpouts, sculpins, and skates (NPFMC, 1994). Breeding occurs in winter, in waters of 500 to 700 m. Eggs in female abdominal brood pouches can number up to 200,000 and can be carried for up to a year before hatching. Larval release may coincide with spring plankton blooms, and the larvae go through several molts before going to the sea bottom as immature crabs (Lewbel, 1983). Hair Crab (Erimacrus Isenbeckii) Korean hair crab, sold commercially by the Japanese, was fished commercially for the first time by the U.S. fleet in 1979. Found primarily near the Pribilof Islands area, this species was used to support an experimental fishery, where crab are shipped live to markets in Japan. Hair crab were first considered as a supplement to ongoing king and Tanner crab operations. Catch quickly increased to about 2.5 million lb by 1980–81 and stabilized at about 1 million lb for the next two years. Beginning in 1983–84, catches have been steadily declining to about 1,000 lb annually beginning in 1988. A similar decline in fishing effort reflects both a decline in the resource as well as poor market conditions. 

BIOLOGY OF HIGHER TROPHIC LEVELS 75 Figure 4.1 Abundance estimates for large male king crabs, Paralithodes camtschatica, from National Marine Fisheries Service trawl surveys in the eastern Bering Sea (solid lines are swept estimates, dotted line is an index based on Japanese catch per unit effort (CPUE), and dashed line is an index based on USSR CPUE). 

BIOLOGY OF HIGHER TROPHIC LEVELS 76 Figure 4.2 Kodiak male red king crab size distribution, for each year from 1974 to 1982 (as determined by research pot sampling; skipmolt crab—the black area—masks new shell crab) (Hayes, 1983). 

BIOLOGY OF HIGHER TROPHIC LEVELS 77 Figure 4.3 Alaska king crab landings from central and western areas (central areas include Prince William Sound, Lower Cook Inlet, Kodiak Island, and South Peninsula; western areas include Bristol Bay, Dutch Harbor, Adak, and the eastern Bering Sea) (Wooster, 1992). Shrimp (Family Pandalidae) Eight pandalid shrimp species representing two genera are taken in commercial and subsistence fisheries off Alaska, but only five are of commercial importance. For many years, shrimp fishermen have targeted primarily pink shrimp (Pandalus borealis), with up to 85 percent of shrimp catch in some years made up of this single species. Other pandalid species, i.e., P. hypsinotus (coonstripe), P. goniurus (humpy), and P. dispar (sidestripe), are most often taken incidental to the fishery for pink shrimp. Humpy and sidestripe shrimp have at times been dominant in trawl catches from specific areas and have supported small fisheries. Other pandalids, i.e., P. danae (dock), P. montagui tridens, P. jordani (ocean pink), and P. platyceros (spot), are also taken incidentally in trawl fisheries. The former two species are the least common of the pandalids found in commercial catches and dock shrimp are rarely taken in Kodiak and the Bering Sea/Aleutian Island regions. Spot and coonstripe shrimp have supported small pot fisheries in Prince William Sound and in the eastern Gulf of Alaska. The extent of pandalid research on Alaskan species has closely followed the rise and fall of the commercial shrimp fishery. As interest in the species grew, government agencies 

BIOLOGY OF HIGHER TROPHIC LEVELS 78 dedicated funds and staff to shrimp research. When the pink shrimp fishery crashed in the mid-1980s, fiscal priorities likewise changed (in this case to king crab) and nearly all shrimp research ended. As a result, most of the literature concerning the life history of pandalid shrimp consists of studies of pink shrimp (P. borealis). Fishery scientists have been working under the assumption that characteristics of pink shrimp life history closely mirror those of other species within the genus Pandalus, while recognizing that regional and species differences likely occur. Balsiger (1981) presents an excellent review of pandalid research. The life history of pink shrimp can be separated into seven distinct development stages. The female carries from 900 to 4,000 developing eggs in her abdomen. Larger, older females normally carry more eggs than do small females (Fox, 1972; Mistakidis, 1957; Haynes and Wigley, 1969). Female pandalid shrimp carry their fertilized eggs until the eggs hatch; thus, mortality to the female precipitates mortality to her egg clutch. Spawning normally occurs in August through October depending on region, with differences in water temperature the apparent controlling factor (Rasmussen, 1969). The incubation stage may last six months. In the Gulf of Alaska, pink shrimp larvae hatch from February through April or early May, whereas other species hatch from April into mid-July (Buck et al, 1975). The unique water circulation patterns of bays and island regions benefit spawning shrimp by preventing planktonic larvae from drifting into unfavorable areas. Larvae are free- swimming for approximately two and one-half months and then settle to the bottom as postlarvae to assume adult behavior. These juveniles are most abundant in waters deeper than 20 fathoms (120 feet). At the onset of winter, however, they appear to migrate to shallow waters of less than 20 fathoms (Buck et al, 1975). Mortality rates are believed to be high for shrimp but are difficult to quantify. Natural mortality estimates have ranged from 22 percent to 85 percent per year, depending on size and age (Gotshall, 1969; Rinaldo, 1976; Anderson, 1978). Predators include cod, sablefish, sole, flounder, halibut, rockfishes, and salmon. One unique aspect of shrimp life history is individual transformation of sex. Almost all shrimp develop as males, although initial development as females has been reported in a few species. Shrimp reach maturity as adult males two years from hatching. At two and one-half years of age, most breed as males, although at three and one-half years a few have already transformed into females. By four and one-half years of age, all shrimp have transformed into sexually mature females. Six months is the average time required for an individual to change sex. Few females live beyond six years. Little is known of the food and feeding habits of pandalid shrimp, but in general they are predators and scavengers. Shrimp feed principally upon a wide variety of organisms, including worms and larvae (Butler, 1964; Fox, 1972; Dahlstrom, 1970). The most common food item identified in studies on shrimp was crab larvae. Mortality rates are believed to be high for shrimp but are difficult to quantify. Natural mortality estimates have ranged from 22 percent to 85 percent per year, depending on size and age (Anderson, 1978; Gotshall, 1969; Rinaldo, 1976). Virtually any large fish in their vicinity, including cod, sablefish, sole, flounder, halibut, rockfishes, and salmon, is a potential predator. Pandalid shrimp species move off the ocean bottom at night. Each species of shrimp differs in the proportion of individuals that migrate upward and in the upward distance of migration (Barr and McBride, 1967). Different species can be found from the surface to at least 230 fathoms (1,380 feet). In the Kodiak and Cook Inlet areas, large concentrations of pink 

BIOLOGY OF HIGHER TROPHIC LEVELS 79 shrimp have been found over sand, silt, or mud substrates. Exploration in more rocky and more difficult trawling areas such as those located in Prince William Sound has been too limited to assess accurately the harvest potential of spot shrimp with trawl gear from these areas. However, it appears that spot shrimp clearly prefer rocky bottoms, usually the bottom of deep canyons or crevices, or pockets along steep, rocky cliffs. As mentioned previously, we understand that Alaska Department of Fish and Game (ADF&G) intends over the short-term to conduct a series of pot surveys on spot shrimp. Scallops (Family Pectinidae) Five species of scallops are commonly found in the Bering Sea and Aleutian Islands area. The most common and the primary target of the commercial fishery is the weathervane scallop (Patinopecten caurinus ). Taxonomic classification and evolutionary relationships among weathervanes and other commercially important scallop species are described by Waller (1991). Weathervane scallops are found in intertidal waters to depths of 300 m (Foster, 1991), but abundance seems to be greatest between the depths of 45 and 130 m on beds of mud, clay, and sand (Hennick, 1973). Little is known about the biology of these species, and according to the North Pacific Fishery Management Council (NPFMC, 1993), there have been no routine biological or fishery programs to sample scallops. Scallops develop through a series of growth stages. In the Atlantic, scallop beds are thought to be strongly affected by ocean current patterns (New England Fishery Management Council, 1982), which in turn can affect local recruitment and settling of larvae; the beds tend to be elongated in the current direction and can include different age and/or size groups (Caddy, 1989; Robert and Jamieson, 1986). Weathervane scallops mature by age three, with rapid growth observed through the first 10 years of life (Hennick, 1973). Scallops are long-lived species and may reach an age of 28 years or more. Principal predators of scallops are various invertebrates (such as crabs and starfish) and fish (such as flatfish). The commercial fishery (a primary source of biological information) has experienced a variable history, during which the fishery exists for a number of years followed by a period of no activity. Alaska scallop resources appear to be healthy, which has stimulated renewed fishery activity. FINFISH Life History, Distribution, and Variability Of the approximately 450 fish, shellfish, and crustacean species in the eastern Bering Sea, only about 25 are commercially important. The discussions that follow provide background data on the known life habits and biological attributes of significant species in the Bering Sea, including their spatial and temporal variability. Information on the commercial industry that depends on some of these species is covered in Chapter 5. A number of previous histories and compilations (e.g., NPFMC, 1993; Lewbel, 1983; Hood and Calder, 1981) were used as references for this section. 

BIOLOGY OF HIGHER TROPHIC LEVELS 80 Most commercial finfish species have experienced some variation in abundance over the years, and in some cases the variability has been extreme. Abundance trends can be measured by a variety of methods. For most species, historical catch statistics and catch per unit effort can be used as measures of relative abundance. Absolute abundance estimates be arrived at only through stock assessment surveys combined with a variety of statistical techniques and modeling. For species such as salmon, run sizes can be determined from a combination of catch and escapement estimates. Most of the information on which these reports and analyses are based is meant to provide advice on the short-term (year-to-year) management of commercial fisheries. Thus, those reports and analyses focus on commercially important species and on the distribution and size of the population or stock. This may not be an appropriate scale at which to approach the kinds of ecosystem questions that this study is asked to address. There is information in these reports and stock assessments, however, which provides insight into ecosystem-scale processes that might be operating in the Bering Sea. Once again, most of the information relates to the eastern Bering Sea and Aleutian Islands, with limited information on the Aleutian Basin (pollock only) and sparse information on the western Bering Sea. In addition, many fish species— especially pelagic species—are not commercially significant and might have significant effects on ecosystem organization. However, little information is available on those species compared with the commercially important ones and we have not discussed them. Details on groundfish1 (excluding halibut) can be found in the NPFMC 1994–95 Stock Assessment and Fishery Evaluation reports for the Bering Sea/Aleutian Islands area and the Gulf of Alaska (NPFMC, 1993). In general both NPFMC and the National Marine Fisheries Service (NMFS) are of the opinion that the groundfish stocks of the eastern Bering Sea/Aleutian Islands are in ''good" condition. This is certainly the case if the resources of the eastern Bering Sea are compared to those of other regions of the world. However, as should be expected for a dynamic system, all species are unlikely to be at their peaks in abundance at the same time. Some species, such as sablefish, offshore pollock in the Aleutian Basin, and Greenland turbot, are currently at relatively low levels. Others, such as a number of flatfish (yellowfin sole, rock sole, arrowtooth flounder, flathead sole, and Alaska plaice) on the eastern Bering Sea shelf and Atka mackerel in the Aleutian Islands are currently at relatively high levels of abundance. Walleye Pollock (Theragra chalcogramma) Walleye pollock is a semidemersal species that inhabits continental slope and shelf waters along the northern rim of the North Pacific, extending from southern Oregon into the southern Chukchi Sea and south along the Asian coast to the southern Sea of Japan (Bakkala, 1993). At present, the walleye pollock stock represents the greatest single-species biomass in the Bering Sea, accounting for approximately 50 percent of the total biomass of all groundfish in the eastern Bering Sea, Aleutian Islands, and Bogoslof district (NPFMC, 1993). They probably account for at least that proportion of the biomass in the western Bering Sea as well (Sabolevsky et al., 1989; Wabkabayashi and Bakkala, 1985). 1 Fish normally caught with bottom-fishing gear, usually bottom trawls. Some of these species (e.g., pollock) also spend time higher in the water column. 

BIOLOGY OF HIGHER TROPHIC LEVELS 81 In the Bering Sea, pollock are found throughout the water column along the eastern and western continental shelves and throughout the deep Aleutian Basin. Massive schools occur on the outer shelf and upper slope from the surface to 500 m. In the eastern Bering Sea, walleye pollock undergo extensive seasonal migrations associated with feeding and reproduction. Overwintering takes place along the outer shelf and upper slope and over deep water where bottom temperatures are relatively high. As temperatures on the shelf rise in spring, part of the walleye pollock population moves to shallower waters (90 to 140 m) to spawn. They first reproduce at the age of three or four years. Spawning occurs primarily in the first quarter of the year in the Aleutian Basin, with major aggregations occurring in the vicinity of Bogoslof Island, and from March through October along the eastern Bering Sea outer shelf (Hinckley, 1986), with major spawning concentrations occurring between the Pribilof Islands and Unimak Island. Along the eastern Bering Sea shelf and slope, each female produces approximately 60,000 to 400,000 pelagic eggs. Fecundity is much lower in the basin. Walleye pollock eggs hatch in two to three weeks, depending on temperature, and larvae tend to inhabit surface waters. Larval pollock begin feeding on copepod eggs and nauplii; as they grow, they feed successively on larger prey such as small copepods. Diets of adult pollock consist mainly of copepods, euphausiids, and fish, the majority of which are juvenile pollock. Pollock are a major part of the diets of northern fur seals and other marine mammals, and are also important prey for many seabirds and fish (Frost and Lowry, 1981b; Pereyra et al., 1976). The population and stock structure of walleye pollock deserves special attention because of its economic and political importance. Much of the literature on stock structure of pollock in the North Pacific is inconclusive. In terms of genetic differences, Bakkala (1993) reported major genetic differences between populations in the Sea of Okhotsk and those in the eastern Bering Sea and Gulf of Alaska. Within North American waters, small but detectable genetic differences were found between pollock from the eastern Bering Sea and the Gulf of Alaska. The genetic relationships among pollock from the eastern Bering Sea, Aleutian Islands, and western Bering Sea are less clear. Dawson (1994) provided an excellent overview of these relationships as well as a clear discussion of the concepts of population and stock with particular reference to Bering Sea pollock. He analyzed several independent data sets, using abundance at age from research and commercial samples, size at age, and morphometric analysis, to assess the degree of isolation of populations of juvenile and adult pollock sampled across all four major areas of the Bering Sea. He concluded that there are several phenotypic stocks of pollock. One is on the eastern Bering Sea shelf, with the main spawning area on the southeastern shelf (southeast of the Pribilof Islands) and with a main juvenile rearing ground on the northeastern shelf (northwest of the Pribilof Islands). Another stock is in the Aleutian Basin with its main spawning ground in the southeast basin near Bogoslof Island. This stock probably occupies the same rearing area as the eastern Bering Sea shelf stock. Dawson's analyses led him to conclude that pollock from the Aleutian Basin and eastern shelf to not move back and forth in large numbers as adults. A third stock was in the Aleutian Islands. Less information was available for western Bering Sea pollock, although Dawson speculated that a fourth stock might be in the southwestern Bering Sea and that pollock in the northwestern Bering Sea in Russian waters might be part of the eastern Bering Sea shelf stock. 

BIOLOGY OF HIGHER TROPHIC LEVELS 82 The relationship between pollock in the Aleutian Basin and the eastern and western Bering Sea shelves is of special interest to fishery scientists and managers. Most important for life history and distribution is the fact that only large, older pollock (older than four years) occupy the pelagic waters of the basin, whereas all ages occupy the shelf and Aleutian Island areas. As Bakkala (1993) pointed out, the absence of juveniles in the basin suggests that these pollock originate, or at least spend their early lives, in other areas, presumably one or more of the shelf areas surrounding the deep basin. Figure 4.4 gives estimates of adult biomass of walleye pollock (ages three and up) in the eastern Bering Sea shelf and Gulf of Alaska from 1964 to 1993. Figure 4.5 gives estimates of pollock year class strength. The most recent surges in pollock biomass, in the late 1970s and early 1980s, represent the very strong 1978 year class in the Bering Sea, and a succession of strong year classes from 1972 to 1979 in the Gulf of Alaska. It appears that the strong 1978 year class accounted for the increase in pollock biomass and resultant catch in the area around Bogoslof Island and the Aleutian Basin (donut hole) (Wespestad, 1993) (Figure 4.6). Although the fishery for pollock has remained relatively constant in time and space, if not in biomass removed, in the Gulf of Alaska, the fishery in the Bering Sea has moved considerably in both space and time (Figures 4.6 and 4.7). Figures 4.8 and 4.9 give the distribution of catch and relative contributions of year classes in the 1970s and early 1980s to the pollock fisheries of the eastern Bering Sea shelf and slope, northwest and southeast of the Pribilof Islands (Francis and Bailey, 1983). The strong 1972 and 1973 year classes appear to have supported the fishery in the northwest in the early and mid-1970s (62 percent of the catch between 1973 and 1977 was taken in the northwest). The strong 1978 year class, in contrast, appears to have supported the fishery in the southeast in the late 1970s and early 1980s (75 percent of the 1982–83 catch was taken in the southeast), as well as the fishery in the Bogoslof and Aleutian Basin areas in the 1980s. Figure 4.10 shows how the center of activity of the pelagic pollock winter trawl fishery moved from the slope around the Pribilof Islands in 1979, to the Unimak/Bogoslof region in 1991 (L. Fritz, personal communication). Not only do the centers of activity of pollock fishing move around from year to year in the eastern Bering Sea (including the basin), within a year the distribution of pollock spawning changes considerably from season to season (Hinckley, 1987; Figure 4.11), moving from the basin in winter to the southeast shelf in spring and up the shelf northwest of the Pribilofs in the summer. Bering Sea pollock are quite different in their population dynamics from Gulf of Alaska pollock. This can be understood best by examining the seasonal, annual, and decadal spatial movements of centers of activities of various life history stages (e.g., spawning and availability of adults to fishing). Pacific Cod (Gadus macrocephalus) Pacific cod also have a broad distribution in the North Pacific, extending along the North American coast from southern California to Norton Sound in the Bering Sea, and along the Asian coast south to the southern tip of the Korean Peninsula and into the Yellow Sea (Bakkala, 1993). This species is common at depths of 80 to 260 m. In the Bering Sea, Pacific cod schools are most abundant on the shelf and upper slope. They migrate seasonally between the 

BIOLOGY OF HIGHER TROPHIC LEVELS 83 Figure 4.4 Estimates of adult (ages three and up) biomass of walleye pollock in the eastern Bering Sea and Gulf of Alaska, 1964–93 (NPFMC, 1993; Bakkala, 1993). "CAGEAN" = catch at-age analysis. 

BIOLOGY OF HIGHER TROPHIC LEVELS 84 Figure 4.5 Pollock year class strength in the eastern Bering Sea and Gulf of Alaska (showing a succession of strong year classes 1972–79 in the Gulf of Alaska) (Wespestad, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 85 Figure 4.6 Walleye pollock catch in the Bering Sea by area, 1964–91 (Wespestad, 1993). Figure 4.7 Eastern Bering Sea pollock catch quarterly distribution (Wespestad, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 86 Figure 4.8 Normalized indices of pollock year-class strength (recruitment at age two) northwest and southeast of the Pribilofs, and for the two areas combined, 1972–79 (Francis and Bailey, 1983). Figure 4.9 Estimates of quarterly catch (1,000 t) of pollock in the eastern Bering Sea northwest and southeast of the Pribilofs, 1973–82 (Francis and Bailey, 1983). 

BIOLOGY OF HIGHER TROPHIC LEVELS 87 Figure 4.10 Pelagic trawl fishery locations (Fritz, in press). Upper panel, 1979; lower panel, 1991. 

BIOLOGY OF HIGHER TROPHIC LEVELS 88 Figure 4.11 Center of activity for pollock fishing (Hinckley, 1987). 

BIOLOGY OF HIGHER TROPHIC LEVELS 89 continental slope and shelf and along the continental slope. Spawning begins in January, but exact timing and areas of spawning are not known. Females produce from 0.2 to 5.7 million eggs, which are benthic and initially slightly adhesive. The eggs hatch within 10 to 20 days, and larvae are distributed at depths from 25 to 150 m, with the largest numbers at 75 to 100 m. Adults are mostly semidemersal and feed on benthic epifauna, planktonic crustaceans such as shrimp and crabs, and juvenile fish such as pollock (Hood and Calder, 1981). Pacific cod are used as food by northern fur seals, halibut, beluga, and sperm whales. Pacific cod is a species that shows significant changes in catch over time, both in the eastern Bering Sea and in the Gulf of Alaska (Figure 4.12). Trends in biomass and recruitment in the eastern Bering Sea fishery are shown in Figure 4.13. The impact of the 1977 year class (recruited at age three in 1980) can be seen in the increase in biomass and fishery production in the early 1980s. Sablefish (Anoplopoma fimbria) Sablefish, also known as black cod, range from the waters off northern Mexico to the northern Bering Sea, and south into Asian waters to the northeast coast of Japan (Bakkala, 1993). Maximum abundance occurs in the Gulf of Alaska. Sablefish occupy the water column from the surface to a depth of 1,200 m, most abundantly between 100 and 1,000 m on the outer continental shelf and continental slope, where 80 to 85 percent of the total species biomass is found. Some sablefish migrate between different areas in the North Pacific; more localized cross-shelf migrations have also been observed. Sablefish spawn during winter (February) at depths of around 550 m, where females release up to 1 million pelagic eggs, which rise toward the surface as they develop and hatch. Later stage larvae are found near the surface. Little is known of egg or larval development, although one- year-old juveniles appear annually in shallow coastal waters. As pelagic juveniles mature, they move into deeper waters and become demersal. Sablefish feed on a wide variety of prey, both pelagic and benthic, depending on location, season, and age of fish. Prey include squid, capelin, pollock, euphausiids, shrimp, pleuronectid species, cottids, and benthic invertebrates. Predators on sablefish include Pacific halibut, ling cod, and sea lions. Atka Mackerel (Pleurogrammus monopterygius) Atka mackerel are distributed from the east coast of the Kamchatka Peninsula, throughout the Komandorsky and Aleutian Islands, north to the Pribilof Islands in the Bering Sea, and east through the Gulf of Alaska as far south as waters off southeast Alaska (NPFMC, 1993). They are most abundant in the Aleutian Islands from Buldir Island to Seguam Pass. Atka mackerel spawn near the bottom. They spawn from June to September in coastal areas with stony or rocky bottoms. The eggs are demersal and are deposited in large masses on stones or in cracks among rocks. Hatched larvae are found at depths of 2 to 30 m and move to the surface at night. The larvae are widely dispersed for distances of up to 200 to 500 miles from shore. Adults feed 

BIOLOGY OF HIGHER TROPHIC LEVELS 90 Figure 4.12 Pacific cod catch (based on unpublished data from the Alaska Fisheries Science Center [AFSC], NMFS, [National Oceanic and Atmospheric Administration]. 

BIOLOGY OF HIGHER TROPHIC LEVELS 91 Figure 4.13 Trends in biomass and recruitment of Pacific cod in the eastern Bering Sea (based on unpublished data from the [AFSC], NMFS, [National Oceanic and Atmospheric Administration]. 

BIOLOGY OF HIGHER TROPHIC LEVELS 92 Figure 4.14 Biomass and recruitment of Atka mackerel (top and middle graphs: NPFMC, 1993; bottom graph: based on unpublished data from [AFSC], NMFS, [National Oceanic and Atmospheric Administration]. 

BIOLOGY OF HIGHER TROPHIC LEVELS 93 largely on euphausiids. Predators on Atka mackerel are marine mammals and the larger pelagic fishes, such as salmon and sharks. Atka mackerel are caught by bottom trawl in depths of 25 to 78 m. Figure 4.14 gives biomass and recruitment trajectories for Atka mackerel in the Aleutian Island area. Because similar stock assessments are not available for Atka mackerel in the Gulf of Alaska, Figure 4.14 also gives catch trajectories for the Aleutian Islands and Gulf of Alaska. Like cod in the eastern Bering Sea, Atka mackerel biomass surged in the Aleutian Islands in the late 1970s and early 1980s as a result of one or two strong year classes (in particular, for the year 1977). Unlike cod, Atka mackerel catch surged once again in the late 1980s and early 1990s (both in the Aleutians and Gulf of Alaska) as a result of a succession of relatively strong year classes. Yellowfin Sole (Limanda aspera) Yellowfin sole are rarely found south of the northern Gulf of Alaska and range through the eastern Bering Sea to the southern Chukchi Sea. Their range continues southward along the Asian coast to Hokkaido Island in Japan and Peter the Great Bay on the Russian coast (Bakkala, 1993). The eastern Bering Sea contains the largest single population of this flatfish, which occurs on the shelf at depths from 5 to 360 m. Yellowfin sole undergo complex seasonal movements (both vertical and horizontal) that are not fully understood. During winter, adults congregate in large, dense schools on the outer shelf and upper slope from 100 to 270 m. In spring, fish begin moving into shallower waters, and by summer the main body of the stock is found on the middle and inner shelf at depths of less than 50 m. At this time of year, feeding and spawning take place. In late autumn, the fish migrate back to deeper waters, apparently to avoid cold bottom water and ice cover. Distribution and movements of yellowfin sole are associated with environmental factors, including ice distribution, temperature, salinity, and bottom sediment type. Adult yellowfin sole are not confined to the bottom, but make periodic vertical movements through the water column. Spawning takes place predominantly in June and July on the inner shelf, with females releasing from 1 million to 3 million pelagic eggs, which accumulate in central areas of well- developed gyres. The larvae are pelagic for four to five months before undergoing metamorphosis; at lengths of about 17 mm, the juvenile sole settle to the bottom along the inner shelf. As the juveniles grow, they apparently move gradually into deeper water. Their principal prey include benthic infauna and epifauna, although they also eat euphausiids, copepods, and fish. Skalkin (1963) suggested that their food sources vary by subregion of the Bering Sea, depth, and season. Important predators of yellowfin sole include Pacific halibut, humans, and northern fur seals (Lewbel, 1983). Greenland Turbot (Reinhardtius hippoglossoides) Greenland turbot has an amphiboreal distribution, occurring in the North Atlantic and North Pacific, but not in the intervening Arctic Ocean (Alton et al., 1988). In the North Pacific, it occurs continuously from the northern Gulf of Alaska through the Aleutian Islands region and eastern and northern Berning Sea into Asian waters south to the Sea of Japan (Bakkala, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 94 Large concentrations of Greenland turbot are found in the eastern Bering Sea and Navarin Basin, at depths of about 70 to 670 m. Seasonal movements by Greenland turbot are complex and not fully understood. They are generally found at shallower depths in the summer than in winter. Spawning occurs from October to December in waters greater than 100 m; the eggs are apparently bathypelagic, developing in deep water. After hatching, the larvae are pelagic and found at 30 to 130 m depth, until they reach a length of about 80 mm, when they transform and become demersal. The overall life history of Greenland turbot is unique among flatfish in that they spend the first three or four years of life on the continental shelf and move to the continental slope where the older juveniles and adults reside (Bakkala, 1993). Greenland turbot feed on a variety of foods, including pelagic, mid- water, and demersal fishes, crustaceans, and squids. Little is known about the predators of Greenland turbot other than humans (Lewbel, 1983). Biomass estimates for Greenland turbot (and arrowtooth flounder, which is discussed further below) and recruitment estimates for Greenland turbot from 1970 to 1993, as shown in Figure 4.15, provide a very interesting contrast. Like the other four flatfish species, they both seemed to respond to the climatic regime shift (discussed in more detail in Chapters 3 and 6) of the late 1970s. Even more interesting is how the distribution of (primarily) juvenile Greenland turbot seems to have been pushed to the northwest along the outer Bering Sea shelf as the ocean climate warned in the late 1970s and early 1980s (Figure 4.16). As was mentioned earlier, Greenland turbot and arrowtooth flounder both occupy continental shelf waters during their first few years as juveniles (Bakkala, 1993) and then deeper waters of the shelf and slope as older juveniles and adults. However, Greenland turbot prefer colder waters than arrowtooth flounder. According to NPFMC (1993), Greenland turbot biomass doubled in size during the 1970s (a very cold period) over early 1960s level. Pacific Halibut (Hippoglossus stenolepis) Pacific halibut ranges from off southern California to as far north as the southern Chukchi Sea along the North American coast and south along the Asian coast to Hokkaido Island, Japan (Bakkala, 1993). Distribution is widespread on the shelf and slope to depths of up to 700 m. These fish undertake seasonal migrations to shallow spring feeding areas and to deeper waters (250 to 550 m) in the fall, where they spawn and remain in the winter. Seasonal movements can extend as far as 800 km. Spawning takes place from November through February, and females release up to two million pelagic eggs. Larvae are also pelagic until they reach a length of about 10 cm after about six months; at that time they settle to the bottom to begin a benthic existence. During the pelagic life stage, eggs and larvae may be transported by currents several hundred kilometers. Pacific halibut are long-lived and may reach ages in excess of 40 years. They are opportunistic feeders, consuming a variety of prey, which varies with age and area. Juvenile fish feed mainly on crustaceans, whereas older fish eat mostly other fish, particularly flounders. Predators of Pacific halibut are poorly known. Bering Sea halibut biomass increased significantly throughout the 1980s, as did recruitment and catch (Figure 4.17). Similar increases were estimated to have occurred over the entire range of the species in the northeast Pacific. The International Pacific Halibut Commission determined that the biomass 

BIOLOGY OF HIGHER TROPHIC LEVELS 95 Figure 4.16 Distribution and density of Greenland turbot on the continental shelf of the eastern Bering Sea, as shown by northwest and AFCC survey data, 1979–86 (Bakkala, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 96 Figure 4.15 Biomass estimates of Greenland turbot and arrowtooth flounder (top graph: based on unpublished data NMFS, NOAA); recruitment estimates for Greenland turbot (bottom graph: NPFMC, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 97 Figure 4.17 Pacific halibut indices of abundance (IPHC, 1994). 

BIOLOGY OF HIGHER TROPHIC LEVELS 98 in the 1980s was at a record high level (IPHC, 1982a). At the end of the decade, halibut abundance entered a period of decline, although large year classes are expected to maintain commercial fisheries near peak levels for some time. Other Flatfishes (Family Pleuronectidae) Other flatfishes of the Bering Sea include rock sole (Lepidopsetta bilineata), flathead sole (Hippoglossoides elassodon), arrowtooth flounder (Atherestes stomias), rex sole (Glyptocephalus zachirus), butter sole (Isopsetta isolepis), longhead dab (Pleuronectes proboscideus ), Dover sole (Microstomus pacificus), starry flounder (Platichthys stellatus), and Alaska plaice (Pleuronectes quadrituberculotus). A few of the more important species are described briefly below. Rock sole range from southern California northward through the Bering and Okhotsk seas and southward to waters off Korea and the Sea of Japan (Bakkala 1993). They are most abundant in the southeastern region of the Bering Sea, where they occupy areas of the shelf with water depths less than 300m. Seasonal movements are not well known. Spawning takes place from March to June at depths near 100 m. Eggs are adhesive and demersal, sinking to the bottom; larvae are pelagic. Adults prey on benthic invertebrates and occasionally on fish. Predators include fish and marine mammals. Flathead sole and a similar form (Bering flounder, Hippoglossoides robustus), range from off northern California to the northern Bering Sea and south to the waters of Japan (Bakkala, 1993). They are most abundant in the eastern portion of the Bering Sea. They range in depth from the surface to 550 m. Seasonal distributions consist of concentrations overwintering in depths of 70 to 400 m on the outer shelf, which then migrate to shallower waters (20 to 180 m) in the spring. Reproduction takes place during February to May within the shelf boundaries; eggs and larvae are pelagic and become widely distributed. The adults prey primarily on benthic crustaceans, mollusks, brittle stars, fish, and squid. Predators of flathead sole are not well known, but are thought to be Pacific halibut and marine mammals. Arrowtooth flounder can be found in waters off central California to the northern Bering Sea. A closely related species, Kamchatka flounder (Atheresthes evermanni), extends south along the Asian coast to the Sea of Japan. The two species may overlap considerably in the eastern Bering Sea and Aleutian Islands (Bakkala, 1993). Arrowtooth flounder are most abundant on the continental slope of the southeastern, central, and northwestern Bering Sea at depths of 200 to 500 m. They move seasonally, from 300 to 500 m depth in the winter, to 200 to 400 m depth in the summer, apparently associated with water temperatures. Adults are thought to spawn from December to February, releasing up to 500,000 bathypelagic eggs. Hatched larvae remain in shallow near shore waters over the shelf for several months and then settle to the bottom (Bakkala and Smith, 1978). Juveniles gradually move into deeper waters as they grow. Major foods include crustaceans and fish, particularly juvenile pollock (Hood and Calder, 1981). Predators on arrowtooth flounder are thought to be Pacific halibut, Greenland halibut, and marine mammals. The catches and estimates of biomass (where and when available) for four flatfish species of commercial importance in the eastern Bering Sea are shown in Figure 4.18. This figure 

BIOLOGY OF HIGHER TROPHIC LEVELS 99 Figure 4.18 Catch and biomass estimates of flatfish of commercial importance in the eastern Bering Sea (NPFMC, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 100 illustrates a number of interesting points. First, yellowfin sole were heavily exploited in the late 1950s and early 1960s, and the population was significantly reduced (NPFMC, 1993). It increased again in the late 1970s and early 1980s. Second, from an ecosystem perspective, note that the biomasses of all four commercially important flatfish species increased significantly in the late 1970s and early 1980s. Figure 4.19 shows estimates of relative changes in flatfish abundance in the Gulf of Alaska between the 1987 and 1990 NMFS triennial trawl surveys. Most striking is the most doubling of the arrowtooth flounder biomass over this period, a pattern similar to that observed in the eastern Bering Sea. Thus, the recent warm regime may have been favorable to most flatfish species of the region, with the exception of Greenland turbot. Greenland turbot seems to prefer colder ocean regimes; it is an amphiboreal species (Alton et al., 1988). Figure 4.19 Gulf of Alaska flatfish relative survey abundance (kg/km 2) (NPFMC, 1993). Pacific Ocean Perch (Sebastes alutus) Pacific Ocean perch range from southern California to the northern Bering Sea and south to northern Honshu Island in Japan (Bakkala, 1993). They are more abundant in the Aleutian Islands region and particularly in the Gulf of Alaska than in the eastern Bering Sea. In the 

BIOLOGY OF HIGHER TROPHIC LEVELS 101 eastern Bering Sea, the species is common in and along canyons and depressions on the upper continental slope. The densest concentrations occur from January to May, during spawning, west of the Pribilofs at depths of 340 to 420 m. During this period, the species undergoes daily vertical migrations, probably for feeding. Because Pacific Ocean perch inhabit such deep waters, tag and recapture studies are virtually impossible. Any statements about their migration patterns are therefore speculation. Pacific Ocean perch are live bearers (as are all rockfishes), and probably mate during the period of October through February. Young are born in springtime (March-June). Larvae at birth are 5 to 8 mm long and are planktonic for an undetermined period of time. The juveniles (ages one to five) feed mainly on copepods and euphausiids; adults feed on euphausiids, copepods, fish, and squid. Predators of this fish are mostly humans and fish, particularly halibut (Pereyra et al., 1976). Figure 4.20 gives biomass trajectories for the Pacific Ocean perch complex,2 and Figure 4.21 gives recruitment time series for the eastern Bering Sea, Aleutian Islands, and Gulf of Alaska. Pacific Ocean perch were heavily fished in the 1960s in the Aleutian Islands, eastern Bering Sea, and Gulf of Alaska regions (as far south as northern Oregon). Populations were severely reduced and, with the exception of the Aleutians, have only recently shown indication of recovery. Rockfish in general, and Pacific Ocean perch specifically, are extreme examples of what Appollonio (1994) refers to as K-selective species. They are very long-lived (some individuals reaching up to 100 years of age) and have low natural mortality rates, and as a result, their populations have very low rates of production. Consequently, any kind of sustained heavy fishing, such as that experienced in the 1960s by the Pacific Ocean perch populations, amounts to mining of the stocks. Other Rockfishes (Family Scorpaenidae) This family of rockfishes includes rougheye rockfish (Sebastes aleutianus ), dusky rockfish (S. ciliatus), northern rockfish (S. polyspinis), shortspine thornyhead (Sebastolobus alascanus), shortraker rockfish (S. borealis), darkblotched rockfish (S. crameri), yelloweye rockfish (S. ruberrimus), and blue rockfish (S. mystinus). Rockfishes are mostly demersal and found from the surface to very deep waters. Little is known about the biology of Bering Sea rockfishes other than Pacific Ocean perch. Pacific Herring (Clupea harengus pallasi) The most widely studied forage (small pelagic) fish in the Bering Sea ecosystem is Pacific herring. This is the only such species for which there is a significant fishery and for which either fishery or survey statistics are collected. Pacific herring range from northern Baja California 2 The Pacific Ocean perch complex is defined as a group of rockfishes including Pacific Ocean perch and northern, rougheye, shortraker, and sharpchin rockfish. These five species are commonly targeted as a group by commercial fishermen. 

BIOLOGY OF HIGHER TROPHIC LEVELS 102 Figure 4.20 Biomass trajectories of age six and older Pacific Ocean perch (NPFMC, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 103 Figure 4.21 Estimated recruitment of two- and three-year-old Pacific Ocean perch for the three regions (NPFMC, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 104 to the Beaufort Sea and south to the coast of Korea (Hart, 1973). They are commonly found throughout the Bering Sea region and in coastal embayments of the Gulf of Alaska. In the eastern Bering Sea, they generally winter northwest of the Pribilof Islands, migrating to the Alaska coast in the spring to spawn from Bristol Bay to the Yukon River (Figure 4.22). This migratory behavior is unique among North American herring stocks. The primary reason for this long-range movement may be to avoid the low water temperatures on the shelf in winter. Herring have been observed to winter north of Norton Sound in brackish lagoons and along the Aleutian Islands, but their numbers suggest they are a relatively small component of the total population. Two other Bering Sea wintering concentrations occur in the Gulf of Olyutorski and off Cape Navarin (Figure 4.22). Spawning occurs from late April to mid-June along the Alaska Peninsula, Bristol Bay, and northeastern Bering Sea. Most herring appear immediately after ice breakup, which would indicate a high tolerance to low temperatures. The arrival at spawning grounds appears to be greatly influenced by climate and oceanographic conditions, particularly the extent and distribution of the Bering Sea ice pack. Herring are substrate spawners, producing as many as 134,000 eggs, and their eggs are highly valued by commercial fishermen. Following spawning, herring appear to remain in coastal waters for feeding. The low abundance of herring in the middle shelf domain may relate to the persistence of cold water in this area in summer (Wespestad, 1991). Offshore migration begins in August (Figure 4.23). Migration pathways may relate to the thermal structure of the eastern Bering Sea. Juvenile herring are planktonic predators, switching to small fishes as they get older. Herring can live as long as 10 years, with sexual maturity occurring by age three or four coinciding with the ages of recruitment to the fishery. Little is known of larval and juvenile stages. Principal predators of herring are kittiwakes, gulls, arctic terns, harbor, ringed, and spotted seals, other fish, and humans (Lewbel, 1983). Estimates of herring biomass and year-class strength from the late 1950s to the mid-1980s are shown in Figures 4.24 and 4.25. Large year classes in the late 1950s supported a brief but very intense winter trawl fishery on the offshore winter grounds. Since then most of the catch has been taken inshore on the spawning grounds. It is interesting that the three largest year classes appear in 1957, 1958, and 1977, years of significant pulse warming in the eastern Bering Sea. It appears that these year classes supported the two major increases in population biomass observed over the last four decades. Pacific Sand Lance (Ammodytes Hexapterus) Pacific sand lance range from southern California to the Chukchi Sea and from Anadyr Gulf as far south as the Sea of Japan (Hart, 1973). Sand lance are small fish and have been found in many areas of the Bering Sea region. They are usually found on the bottom, at depths between 0 and 100 m, except when engaged in pelagic feeding on crustaceans and zooplankton. Spawning is believed to occur in the winter. Sand lance mature at ages two to three and lengths of 10 to 15 cm. Little is known about their seasonal distribution and abundance. They are rarely captured in commercial or survey trawls. In the Bering Sea, sand lance have been commonly found in the stomachs of salmon, northern fur seals, and many species of marine birds. 

BIOLOGY OF HIGHER TROPHIC LEVELS 105 Figure 4.22 Winter grounds of major Bering Sea herring concentrations (large arrows from Soviet data; vertical stripes from Japanese catch data; small arrows inferred migration) (Barton and Wespestad, 1980). Figure 4.23 Migration routes to the eastern Bering Sea winter grounds from coastal spawning sites as inferred from fishery and research catches (Wespestad, 1991). 

BIOLOGY OF HIGHER TROPHIC LEVELS 106 Figure 4.24 Estimated biomass of herring ages three to nine in the eastern Bering Sea, 1959–88, as estimated by cohort and catch at age analysis Wespestad, 1991). Figure 4.25 Estimated abundance of Pacific herring in the eastern Bering Sea at age one, 1958–84, as estimated by cohort and catch at age analysis (estimates are deviations from the geometric mean year class) (Wespestad, 1991). 

BIOLOGY OF HIGHER TROPHIC LEVELS 107 Capelin (Mallotus villosus) Capelin are widely distributed in the Gulf of Alaska, Bering Sea, and Sea Okhotsk, and along the Kamchatka Peninsula. They range from Juan de Fuca Strait through arctic Alaska and south to the Korean coast (Hart, 1973). A member of the smelt family, capelin have been known to be very abundant in the Bering Sea. In the North Pacific, they can grow to a maximum of 25 cm at age four. Most capelin spawn at ages two to three. Spawning occurs in spring in intertidal zones of coarse sand and fine gravel. In the Bering Sea, adult capelin are found near shore only during the months surrounding the spawning run. At other times of the year, capelin are found far offshore in the vicinity of the Pribilof Islands and the continental shelf break. Their seasonal migrations may be associated with the advancing and retreating polar ice front in the Barents Sea. Capelin (and other smelts, including rainbow smelt and eulachon) are commonly found in the stomachs of seabirds, marine mammals (particularly those feeding along the ice edge), and forage fishes, and therefore are believed to be important prey when abundant (Anonymous, 1993). Few data exist on distribution or abundance trends in capelin and other smelt species. Figure 4.26 shows what is known about their distributions and Figure 4.27 shows their abundances (capelin and eulachon only). Indications are that both capelin and eulachon may have declined significantly in the 1980s. Pacific Salmon (Oncorhynchus spp.) All five Pacific salmon species are found in the Bering Sea area. Sockeye salmon (O. nerka) is the most common, and Bristol Bay supports the largest sockeye fishery in the world. Chinook (O. tshawytscha) , chum (O. Keta), coho (O. kisutch), and pink (O. gorbuscha) salmon are all found in lesser degrees of abundance. Much has been written describing the life history and distribution of Pacific salmon in the North Pacific region (Groot and Margolis, 1991). Depending on the species, juvenile salmon migrate from their freshwater rearing areas between birth and age two. Once in the marine environment, juvenile fish follow an annual migration pattern that takes them away from the coast and into the Bering Sea and North Pacific Ocean. Once the fish achieve the proper age and size for reproduction, they return to their freshwater streams of origin to spawn, an event that takes place between early summer and early winter. After spawning, all salmon of these five species die. Ages of adult fish range from two to six years, depending on species and population. Smolt out migration from rivers occurs in the spring and summer following ice breakup. Returning adult salmon migrate into coastal areas during the summer months where they support large commercial and subsistence fisheries. During their oceanic lives, salmon live on zooplankton, squid, crab larvae, and other fish. Predators in the oceans include seals, killer whales, and humans. During spawning returns to land, salmon are preyed on by bears, other large mammals, and humans (Lewbel, 1983). The long-term dynamics of Pacific salmon production in the eastern Bering Sea (and Alaska region in general) has been well documented by Francis and Hare (1994). Further discussion is given in Chapter 5. Those studies have shown that salmon production in the northeast Pacific exhibits time and space variability that is closely linked to similar dynamics 

BIOLOGY OF HIGHER TROPHIC LEVELS 108 Figure 4.26 Generalized distribution of smelts in the eastern Bering Sea based on NMFS groundfish trawl surveys and fisheries observer data (Os and Is represent outer and inner shelf areas, respectively, over which fisheries observer data are pooled for analysis of eulachon abundance trends) (upper figure: Fritz et al., 1993; lower figure: Hinckley, 1987). 

BIOLOGY OF HIGHER TROPHIC LEVELS 109 Figure 4.27 Trends in capelin abundance in the Pribilof Islands region (Hunt et al., 1981b) and in the Gulf of Alaska (Piatt and Anderson, in press), and trends in CPUE (catch per unit effort) of eulachon from fisheries observer data on outer and inner shelf areas of the eastern Bering Sea (hours represent total duration of sampled trawls in region for each year) (Anonymous, 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 110 in the North Pacific atmosphere and ocean physics. Estimates of salmon production (catch plus escapement for the three major species—chum, sockeye, and pink) for the eastern and western Bering Sea for 1952–91 (Figure 4.28) are based on estimates of Rogers (1992). Estimates of production for the western Bering Sea (Rogers, 1992) are production statistics for Russia, adjusted by the estimated mean ratios of eastern Kamchatka to total USSR catches for 1952–75 from the International Pacific Fisheries Commission (1979) (sockeye, 33 percent; pink, 18 percent; chum, 14 percent). These data illustrate that there was an enormous increase in eastern Bering Sea production in the late 1970s. Eastern Bering Sea salmon production is dominated by sockeye, whereas western Bering Sea production is dominated by pink salmon. Summaries of recent trends in fish populations and biomass are given in Table 4.1, Table 4.2, and Figure 4.29. BIRDS Life History and Distribution Thirty-six species of seabirds nest in Alaska, with 32 of them nesting on the coast of the Bering Sea and Gulf of Alaska; an additional three species nest elsewhere but spend significant parts of the year in the Bering Sea and Gulf of Alaska (Table 4.3). There are also 12 species of sea ducks (Table 4.4) and five species of geese (Table 4.5) that nest near the coast or on islands of the Bering Sea, or winter in the Bering Sea and Gulf of Alaska. In addition, there are a wide variety of other species of seabirds, waterfowl, shorebirds, and others such as raptors that inhabit or migrate through the region during the year; many of the most important have been described (Hood and Calder, 1981; Lewbel, 1983; NPFMC, 1993; USFWS, 1989). Distributions and presence of these migratory and nonmigratory species are based on species evolution, geology and geography, and climate (Hood and Calder, 1981). Bird habitats of the Bering Sea region include near shore waters, lagoons, unvegetated intertidal areas (such as the outer Yukon delta), and vegetated intertidal areas. Shore and waterbirds tend to move north in the spring as part of a great migration, where they await the ice breakup. The search for nesting grounds occurs both on the margins of the Bering Sea and the lands of the American and Asian continents. With freeze- up in the fall, the migratory birds move from northern wetlands to the marine habitats in the south. The seabirds of the region include such families as Diomedeidae, Procellariidae, Hydrobatidae, Phalacrocoracidae, Laridae, and Alcidae. These include the albatrosses, shearwaters, fulmars, storm petrels, cormorants, pelagic gulls (kittiwakes), murres, guillemots, auklets, murrelets, and puffins. In addition, there are a wide variety of other species of seabirds, waterfowl, shorebirds, and others such as raptors that inhabit or migrate through the region during the year. Waterfowl are members of the family Anatidae, which includes geese, ducks, and swans. The shorebirds are members of the families Charadriidae, Scolopacidae, and Phalaropodidae; these include wading birds, such as turnstones, godwits, curlews, plovers, dowitchers, and other sandpipers. Other important birds that nest and feed along the margins of the Bering Sea include the bald 

BIOLOGY OF HIGHER TROPHIC LEVELS 111 Figure 4.28 Estimated salmon production (catch and escapement) for eastern and western Bering Sea, 1952–91 (based on unpublished data, from Alaska Fisheries Science Center, NMFS [National Oceanic and Atmospheric Administration]. 

BIOLOGY OF HIGHER TROPHIC LEVELS 112 Table 4.1 Total allowable catch quota or harvest prediction, actual harvest, and current status of major resources in the exclusive economic zone off Alaska, 1995 TOTAL ALLOWABLE CATCH AND HARVEST (1) STATUS OF RESOURCE SPECIES 1995 1995 1994 1994 1995 CONDITION TREND IN BIOMASS ABC TAC/Pred HARVEST TAC/Pred OF RESOURCES (6) (2) (2) RESOURCE ABUNDANCE Pollock 9,264,000 1,394,060 1,496,750 1,482,676 1,372,960 EBS/Al- EBS/Al- Average, Stable, GOA- GOA-Low Decreasing Pacific cod 2,193,000 397,200 241,400 244,148 319,200 EBS/Al- EBS/Al- Average, Increasing, GOA-High GOA- Decreasing Flatfish 9,622,470 1,303,990 378,525 298,249 401,167 EBS/Al- EBS/Al- Very High, Increasing, GOA- GOA- Unknown Uncertain Rockfish 1,020,111 50,265 43,207 35,192 41,648 EBS/Al- EBS/Al- Low, GOA- Stable, GOA- Low Increasing Sablefish 225,300 25,300 28,840 23,905 25,300 EBS/Al- EBS/Al- Average, Increasing, GOA- GOA-Stable Average Atka 846,000 128,240 71,505 73,120 83,240 EBS/Al- EBS/Al- Mackerel High, GOA- Stable, GOA- Unknown Uncertain Other 682,000 30,710 39,581 28,556 34,226 EBS/Al- EBS/Al- Groundfish High, GOA- Increasing, Unknown GOA- Uncertain Total 23,831,881 3,329,765 2,299,808 2,185,846 2,277,741 EBS/Al- EBS/Al- Groundfish High, GOA- Stable, GOA- Low Stable/ Decreasing Halibut (8) 87,906 17,282 21,500 20,679 17,245 EBS/Al- EBS/Al- Avg, GOA- Decreasing, Avg GOA- Increasing Salmon (3) (4) (4) 167,000,000 197,000,000 147,000,000 EBS/Al- EBS/Al- High, GOA- Stable, GOA- High Stable/ Decreasing King Crab (4) (4) (4) 3,865 (4) EBS/Al-V. EBS/Al- (5) Low, GOA- Decreasing, V. Low GOA-Stable Tanner (4) (4) 72,065 73,155 (4) EBS/Al- EBS/Al- Crab (9) Avg, GOA- Decreasing, Low GOA-Stable Dungeness (4) (4) 1,987 635 1,500 GOA-Avg/ GOA-Stable Crab Low Pink (4) (4) 900 1,179 1,200 EBS/Al-V. EBS/Al- Shrimp Low, GOA- Stable, GOA- V. Low Stable Herring (7) (4) (4) 61,741 43,401 44,270 EBS/Al- EBS/Al- High, GOA- Stable, GOA- Avg Stable Note 1: Unless otherwise indicated quotas and harvest values are given in metric tons. Note 2: Total groundfish TAC includes reserves for all species. Note 3: Salmon predicted and actual run size and catches given in number of fish. Note 4: Prediction and/or mid-season quotas not available for all Alaska areas. Note 5: Combines calendar year and split year seasons for some species. Note 6: Exploitable biomass for some species unknown. Note 7: Includes roe and roe on kelp harvests & predictions in short tons. Note 8: Exploitable biomass and harvest of halibut for Alaska only. Note 9: Includes 1993/94 T. bairdi and excludes Nov/Dec 1994 T. bairdi catch. Source: Based on data from NMFS, ADF&G, and Committee on the Bering Sea Ecosystem. 

BIOLOGY OF HIGHER TROPHIC LEVELS 113 Table 4.2 Total allowable catch or harvest prediction, actual and current status of major resources in the eastern Bering Sea/Aleutian Islands, 1995 TOTAL ALLOWABLE CATCH AND HARVEST STATUS OF RESOURCE (mt) SPECIES 1995 1995 1994 1994 1995 CONDITION TREND IN BIOMASS ABC TAC (2) HARVEST TAC (3) OF ABUNDANCE (1) RESOURCE Pollock 8,080,000 1,250,000 1,330,00 1,313,135 1,250,000 Average Stable (EBS) (AI) 189,000 56,600 56,600 57,097 56,600 Average(?) Stable(?) Bogoslof 442,000 22,100 850 922 1,000 Low Stable (518) Pacific cod 1,620,000 328,000 191,000 196,569 250,000 Average Increasing Yellowfin 2,770,000 277,000 170,325 144,544 190,000 High Increasing Sole Greenland 150,000 7,000 7,000 10,321 7,000 Low Declining Turbot Arrowtooth 625,000 113,000 10,000 14,366 10,227 High Increasing Flounder Rock Sole 2,330,000 347,000 63,750 60,544 60,000 High Increasing Flathead 725,000 138,000 (4) (4) 30,000 High Stable Sole Other 677,000 117,000 47,600 29,766 19,540 High Stable Flatfishes Sablefish 16,500 1,600 540 699 1,600 Low Increasing (EBS) (AI) 13,900 2,200 2,800 1,745 2,200 Average Declining Pacific 47,100 1,850 1,910 1,906 1,850 Low Stable Ocean Perch (EBS) (AI) 252,000 10,500 10,900 10,932 10,500 Low Stable Other POP 29,700 1,400 1,190 127 1,260 Unknown Unknown Complex (EBS)(4) Sharp/ 94,500 5,670 5,670 5,090 5,103 Unknown Unknown Northern (AI) Short/ 45,000 1,220 1,037 935 1,098 Unknown Unknown Rougheye (AI) Other 7,300 365 310 133 329 Average Stable Rockfish (EBS) (AI) 15,500 770 655 297 693 Average Stable Atka 825,000 125,000 68,000 69,559 80,000 High Stable Mackerel Squid Unknown 3,110 2,644 588 1,000 Unknown Unknown Other 682,000 27,600 22,432 24,518 20,000 High Increasing Species Total 19,636,500 2,836,985 1,995,213 1,943,793 2,000,000 High Stable Groundfish Note 1: Exploitable biomass for some species unknown. Note 2: 1994 TAC includes the final allocated portion of the 15% reserve allocation & CDQ quota and catch. Note 3: 1995 TAC includes the 15% reserve allocation. Note 4: Flathead sole was grouped with other flatfish in 1994 allocation. Source: based on data from NMFS, ADF&G, and the Committee on the Bering Sea Ecosystem. 

BIOLOGY OF HIGHER TROPHIC LEVELS 114 Figure 4.29 Trends in fish populations and biomass (based on data from NMFS, ADF&G, and the Committee on the Bering Sea Ecosystem). 

BIOLOGY OF HIGHER TROPHIC LEVELS 115 Table 4.3 Numbers of seabirds and seabird colonies in Alaska. Species Number of Sites Catalog Total Estimated Total Northern fulmar 30 1,451,980 2,000,000 Sooty shearwater 0 - 21,000,000 Short-tailed shearwater 0 - 20–80,000,000 Fork-tailed storm petrel 60 1,148,500 5,000,000 Leach's Storm petrel 38 1,709,600 4,000,000 Double-crested cormorant 82 4,701 7,000 Brandt's cormorant 1 11 100 Pelagic cormorant 285 40,888 90,000 Red-faced cormorant 179 51,613 130,000 Pomarine jaeger - - ? Parasitic jaeger - - ? Long-tailed jaeger - - ? Bonaparte's gull - - ? Mew gull 44 3,442 10,000 (?) Herring gull 12 28 300 (?) Glaucous-winged gull 547 229,022 500,000 Glaucous gull 115 5,719 30,000 Black-legged kittiwake 263 1,752,906 2,500,000 Red-legged kittiwake 6 226,802 250,000 Ross's gull 0 - 20–30,000 Sabine's gull - - ? Arctic tern 131 13,586 25,000 Aleutian tern 28 3,403 10,000 Dovekie - - 100 Common murre 42 1,690,584 5,000,000 Thick-billed murre 76 1,768,536 5,000,000 Black guillemot 12 323 400 Pigeon guillemot 363 40,571 200,000 Marbled murrelet ? ? 250,000 Kittlitz's murrelet ? ? 100,000 Ancient murrelet 40 113,302 400,000 Cassin's auklet 21 319,140 600,000 Parakeet auklet 125 429,436 800,000 Least auklet 31 3,432,068 6,000,000 Whiskered auklet 10 6,400 20,000 Crested auklet 38 1,343,750 2,000,000 Rhinoceros auklet 12 112,618 200,000 Tufted puffin 502 2,108,535 4,000,000 Horned puffin 435 768,011 1,500,000 Source: Sowls et al. (1978). 

BIOLOGY OF HIGHER TROPHIC LEVELS 116 

BIOLOGY OF HIGHER TROPHIC LEVELS 117 eagle, peregrine falcon, sandhill cranes, Aleutian tern, and McKay's bunting. Brief descriptions of the principal bird species undergoing population fluctuations of note are presented. Table 4.5 Trends in the abundance of geese nesting and wintering in the eastern Bering Sea Species Nesting Wintering Status Greater white-fronted goose + Increasing Emperor goose + + Decreasing Brant + Decreasing Cackling Canada goose + Increasing Aleutian Canada goose + Increasing Source: Springer (1993). Diets of the seabirds range from almost entirely zooplankton to primarily fish; there are no strictly piscivorous seabirds. All of them consume many types of prey but most actually depend on only a few kinds of zooplankton, squids, and fishes (Hatch, 1984; Hatch and Sanger, 1992; Hunt et al., 1981a; Sanger, 1986; Springer and Roseneau, 1985; Springer et al., 1984, 1986, 1987). Important zooplankton are large calanoid copepods, euphausiids, and hyperid amphipods. Most of the fishes consumed by seabirds are pelagic species, including primarily lanternfish, sand lance, capelin, greenlings, arctic cod (Boreogadus saida) saffron cod, and pollock. Wintering sea ducks and emperor geese feed mainly on invertebrates, particularly mollusks and crustaceans. Sources and Magnitude of Variability Mass mortalities and major declines in the abundance of marine birds in Alaska have been documented in the past 200 years and have had numerous causes, including predation by introduced mammals, oiling, drowning in drift nets, and hunting. Since the early to mid-1970s, when widespread, systematic studies of seabird colonies were initiated, fluctuations in population sizes and productivity have been common. Recent changes have been both downward and upward. Prey Availability The population dynamics of seabirds in general appears to be governed primarily by the availability of prey (Furness and Monaghan, 1987); productivity of seabirds is sensitive to food supply, and population abundance fluctuates in response to trends in recruitment. The failure of prey resources can lead to mass mortalities of seabirds that can cause or contribute to population declines, while increases of prey can cause increases in seabird survival and 

BIOLOGY OF HIGHER TROPHIC LEVELS 118 populations. Papers in Croxall (1987) demonstrate the impacts of commercial fisheries on seabird food availability, citing the experience of various species declines offshore California, Salvador, and Norway. In the Norwegian case, for example, Atlantic puffins, common guillemots, and razorbills suffered drastic breeding reductions due to intensive herring fishing from 1958 to 1969. Productivity Seabird productivity depends on prey being adequate for females to lay eggs, for the eggs to be incubated successfully, for healthy chicks to be raised, and for the juvenile birds to make the transition to independence, which includes surviving through the winter. Insufficient prey at any one of these stages, which span an interval of up to approximately eight months, can dramatically reduce productivity. Productivity of seabirds varies greatly between years and over longer intervals. For example, kittiwake productivity on the Pribilofs during just the first half (laying-fledging) of the critical period has varied by nearly two orders of magnitude between years (Dragoo and Sundseth, 1993). Interannual variability in productivity of kittiwakes is common elsewhere in Alaska, as it is for murres, cormorants, and other species (Hatch, 1993; Hatch et al., 1993; Murphy et al., 1986, 1991; Springer, 1991). Years of poor productivity are characterized by small clutch sizes, nest abandonment, and chick starvation, all of which are indicative of food stress. Die-Offs At least five large wrecks, or die-offs, of seabirds have occurred in the past decade in the Bering Sea and Gulf of Alaska—in 1983, 1984, 1989, 1991, and 1993 (Nysewander and Trapp, 1984; Piatt and van Pelt, 1993; Piatt et al., 1990; A.M. Springer, unpublished data). Estimates of the numbers of birds (including murres, black- legged kittiwakes, and shearwaters) that died in each range from 10,000 to 100,000. The most likely cause in all years but 1984 was starvation. The die-off in 1984 was reported only from St. Lawrence Island and apparently was not caused by starvation, although the exact cause is not known (A.M. Springer, unpublished data). The only reported die-off of a similar magnitude before 1983 was in 1970 (Bailey and Davenport, 1972). There are no estimates of the effects that any of the die-offs might have had on regional abundances of seabirds. It is improbable that changes in numbers at nesting colonies could be detected following particular die- offs, because they occurred either in winter or over a broad area, or both, and thus likely included birds from numerous nesting locations. The cumulative effect, however, might have contributed to an apparent widespread decline in murre populations in the Gulf of Alaska (Piatt, 1994). 

BIOLOGY OF HIGHER TROPHIC LEVELS 119 Abundance Change in the abundance of seabirds in Alaska appears to be the norm (Table 4.6), and it seems likely that most declines result from decreased productivity, including the survival of juvenile birds through their first winter. There are no known catastrophic declines for entire species over short intervals that can be attributed to wrecks. Rather, all of the declines have had a similar, gradual rate averaging 4.4 percent per year (N = 19, S = 2.1 percent per year). In contrast, increases in numbers have been both gradual and extreme. Of 23 recorded occasions when numbers have increased, the rates have been greater than about 20 percent per year in 10 cases, with a high of 78 percent per year for common murres at Middleton Island between 1956 and 1974. That change and the growth in numbers of black-legged kittiwakes (+26 percent per year) and glaucous-winged gulls (+50 percent per year) on Middleton Island likely resulted in large part from immigration following the creation of extensive nesting habitat by the earthquake of 1964. Likewise, other cases of rapid colony growth—of thick-billed murres (+19 percent per year) and black-legged kittiwakes (+38 per year) at Buldir Island, black-legged kittiwakes at Margerie Glacier in Glacier Bay (+30 per year), and northern fulmars at St. George Island (+25 percent per year) —probably were accounted for in part by immigration. Nur and Ainley (1992) concluded that seabirds can be divided into two groups based on maximum potential population growth rate from productivity alone: species with an upper-quartile growth rate of around 19 percent or more and those with an upper-quartile rate of 13 percent or less. The first group includes species that lay many eggs in each clutch, such as cormorants and gulls. The second group includes species that lay just one or two eggs, such as murres and kittiwakes. Among species in these groups, immigration is the cause for populations that exhibit growth rates greater than the upper theoretical limit. There are other cases where colony growth has been more gradual. Because of the important role that immigration can play, however, it is difficult to estimate the relative contributions of productivity and immigration. Growth from immigration consists primarily of the recruitment of prebreeders from other locations; adult birds generally have high fidelity to their nesting colonies. Thus, emigration would not be expected to rapidly deplete colonies in the same way that immigration can swell their ranks. The concern over seabird population trends has an important spatial context, namely, the decline of five piscivorous species on the Pribilof Islands. In general, those declines contrast with stable or increasing populations of seabirds elsewhere in the Bering Sea. Red-faced Cormorant (Phalacrocorax urile). Whereas there are three species of cormorants in the Bering Sea region, the red-faced cormorant is found mostly in the Aleutian Islands and Alaska Peninsula. Its breeding range is from the Komandorsky Islands through the Aleutians, to the Pribilofs, and east along the Gulf of Alaska coast to Prince William Sound (Kessel and Gibson, 1978; Sowls et al., 1978). Nests are usually found along lower cliff faces and constructed of seaweed, with clutches of two to three eggs on St. Paul Island and with broods of up to four found in the western Aleutians (Dick and Dick, 1971; Hunt et al., 1981b; Trapp, 1975). Red- faced cormorants live all year on the Pribilofs, feed near shore, and do not hunt more than a few kilometers from their nesting area, though they may venture out into open water in the spring and fall. They obtain their prey— fish (primarily sculpins), shrimp, crabs, and 

BIOLOGY OF HIGHER TROPHIC LEVELS 120 Table 4.6 Trends in the abundance of seabirds in Alaskaa Species/Location Range of Years Trend Rate (% / y) Reference Northern Fulmar St. George I. 1976–1988 0 Dragoo and Sundseth, 1993 1988–1992 up 100% 25 St. Paul I. 1976–1992 up 230% 38 L. Climo and A. Golovkin, unpubl. data Semidi Is. 1976–1989 up 40% 3.1 Dragoo and Bain, 1990; Hatch, 1992 Pelagic Cormorant Cape Thompson 1960–1977 down 40% 2.4 Springer et al., 1985 Middleton I. 1974–1991 up 100% 5.9 Gould et al., 1984; S. Hatch, unpubl data Red-faced Cormorant St. Paul I. 1976–1992 down 70% 4.4 L. Climo and A. Golovkin, unpubl. data Glaucous-Winged Gull Middleton I. 1955–1974 up 900% 47 S. Hatch, unpubl. data 1974–1991 up 900% 53 S. Hatch, unpubl. data Black-legged Kittiwake Cape Lisburne 1977–1985 up 27% 3.4 Springer et al., 1985; unpubl. data Cape Thompson 1960–1976 down 45% 2.8 Springer et al., 1985 1976–1990 up 300% 2.1 Springer et al., 1985; Sharp, 1991 Bluff 1975–1992 0 Murphy et al., 1992; unpubl. data Nunivak I. 1987–1990 0 McCaffery, 1989 St. Paul I. 1976–1992 down 50% 3.1 Climo, 1993 St. George I. 1976–1984 down 50% 6.3 Dragoo and Sundseth, 1993 1984–1992 up 30% 3.8 Dragoo and Sundseth, 1993 Cape Peirce 1976–1993 up 22% 2.2 Haggblom, 1994 1986–1992 0 Agattu I. 1975–1985 up 66% 6.6 Williams and Byrd, 1992 1985–1991 0 Williams and Byrd, 1992 Buldir I. 1974–1988 up 530% 38 Williams and Byrd, 1992; Williams and Byrd, Unpub. data 1988–1992 0 Williams and Byrd, 1992; Williams and Byrd, unpubl. data Kiska I. 1978–1988 up 38% 3.8 V. Byrd, unpubl. data Semidi Is. 1973–1989 0 Hatch et al. 1993 Chiniak Bay 1975–1984 up 200% 22 Hatch et al. 1993 1984–1989 0 Hatch et al. 1993 Chiswell Is. 1976–1991 0 Nysewander and Dipple, 1992 Barren Is. 1977–1991 0 Nysewander and Dipple, 1992 Puale Bay 1976–1991 0 Nysewander and Dipple, 1992 Prince William Sound 1973–1989 0 Irons et al., 1987; unpubl. data Middleton I. 1956–1975 up 500% 2.6 Gould et al. 1984 1975–1989 down 40% 2.9 Gould et al. 1985; Hatch et al. 1993 Margerie Glacier 1967–1983 up 500% 31 Climo and Duncan, 1991 1983–1991 up 230% 29 Climo and Duncan, 1991 Boussole head 1974–1991 down 70% 4.1 Climo and Duncan, 1991 Cenotaph I. 1976–1989 down 100% 7.7 Climo and Duncan, 1991 Source: Committee on the Bering Sea Ecosystem a This table does not include information on changes in numbers of seabirds on islands where foxes were introduced. 

BIOLOGY OF HIGHER TROPHIC LEVELS 121 amphipods—by pursuit diving close to shore and near the sea bottom (Ashmole, 1971; Hunt et al., 1981b). The number of nests on St. Paul Island has declined by an estimated 70 percent since the mid to late 1970s (Table 4.3). In contrast, red-faced cormorants apparently have expanded their range into Prince William Sound in recent years—none were found until 1969 and they are now numerous (Kessel and Gibson, 1978). Information on trends is lacking for all other colonies. Black-legged Kittiwake (Rissa tridactyla). Black-legged kittiwakes are probably the most widely distributed of the seabirds in Alaska. They are pelagic gulls that are found across the Arctic and are numerous in the eastern Bering Sea. Their nests, made of vegetation and mud, are found on cliff ledges and sometimes slopes if ground predators are absent. Numbers of eggs laid are one to three (Hunt et al., 1981a). The pelagic density of this species is dispersed and low. Most of the breeding population leaves the Bering Sea in winter, though some individuals are still found ranging from the Aleutians to the Pribilofs (Shuntov, 1972). With respect to feeding method, black-legged kittiwakes mostly dip, though they are also known to surface seize or use shallow pursuit diving (Hunt et al., 1981). The principal food is fish (cod, myctophids, sand lance, and capelin), but also includes crustaceans and cephalopods. On St. George Island, numbers of black-legged kittiwake fell sharply between 1976 and 1984, but have been recovering since then, while on St. Paul Island the decline continued through at least 1989 (Table 4.3). These are the only locations known in the Bering Sea where black-legged kittiwakes are known to be less abundant now than in the past. In contrast, black-legged kittiwakes have increased dramatically since the 1970s at all three colonies where they have been censused in the western Aleutians—Buldir Island (+530 percent), Agattu Island (+50 percent), and Kiska Island (+38 percent). Black-legged kittiwakes on or near the coast of the eastern Bering Sea—Bluff (Norton Sound), Nunivak Island, and Cape Peirce (Bristol Bay)—have been stable since the mid-1970s, notwithstanding considerable interannual variability at Bluff. Likewise, numbers have also been stable or increasing at most colonies in the eastern Chukchi Sea and Gulf of Alaska. Kittiwakes are known to have declined only at Middleton Island in the eastern Gulf of Alaska, about 40 percent since the early 1980s following a fivefold increase between the mid-1950s and mid-1970s, and at two very small colonies, Boussole Head and Cenotaph Island, in southeastern Alaska, at the edge of the species range. Nearby in Glacier Bay, however, kittiwake numbers at the largest colony in southeastern Alaska have increased by an order of magnitude since the early 1970s (Climo and Duncan, 1991). Red-legged Kittiwake (Rissa brevirostris). Red-legged kittiwakes are endemic to the Bering Sea and are known to nest at only four locations in the world—the Pribilof Islands, Bogoslof Island, Buldir Island, and the Komandorsky Islands (Byrd, 1978). This species of kittiwake nests on cliffs, sheltered ledges and smaller ledges than do black-legged kittiwakes. Their nests usually have just one egg (Hunt et al., 1981b). During the summer, red-legged kittiwakes can be found on the shelf break adjacent to the Pribilofs, and seldom in water shallower than 100 m. In the fall and winter, most of the birds leave the Bering Sea (Kessel and Gibson, 1978). They feed by dipping or surface seizing (Ashmole, 1971), and much of this activity takes place at night. 

BIOLOGY OF HIGHER TROPHIC LEVELS 122 According to Hunt et al., (1981b), myctophids (lantern fish) are an important food for this kittiwake, which also consumes pollock and cephalopods. The total nesting population of red-legged kittiwakes was approximately 230,000 in the mid-1970s, with about 95 percent nesting on St. George Island. Numbers have declined by about 40 to 60 percent on the Pribilofs since then (Table 4.3), and this seabird is now a candidate for protection under the Endangered Species Act (Byrd, 1994). However, like black-legged kittiwakes, red-legged kittiwakes also have increased dramatically on Buldir Island since the mid-1970s (Byrd, 1994). Common and Thick-billed Murre (Uria lomvia and U. aalge). Murres are also widely distributed throughout Alaska, with a total population on the order of 10 million individuals about evenly divided between the two species. These birds are found in the Bering Sea, northern Pacific, and North Atlantic. The greatest concentrations of murres in the Bering Sea region are on the Pribilof Islands, St. Matthew Island, St. Lawrence Island, the Semidi Islands, and the Cape Peirce-Cape Newenham region. Common murres are found mostly on the mainland coasts. These birds tend to nest in mixed colonies. Both species lay a single egg on bare cliff rocks, but the common murres prefer broader ledges and flatter areas that the narrow cliff ledges preferred by thick- billed murres. Juvenile birds jump from their cliff nests into the water at three weeks of age and stay in the water for another three weeks before they can fly. Murres are long-lived birds and begin mating at five years of age. They migrate north in April following leads along the northern Bering and into the Chukchi Sea, and then return to colonies for mating. In the fall, they are found offshore, from Bristol Bay to the Gulf of Anadyr, until forced southward by the ice front (Shuntov, 1972). When the ice has advanced well into the Bering, the murres are found primarily in the extensive shelf areas of the southern Bering Sea. Murres obtain food by diving to depths of up to 130 m (Forsell and Gould, 1981), where they catch fish and invertebrates. Thick-billed murres have a more varied diet and venture farther from shore than common murres; common murres tend to feed on near shore mid-water fish, such as cod, sand lance, capelin and pricklebacks, whereas thick-billed murres also depend on demersal fishes, such as sculpins and invertebrates (Hunt et al., 1981a; Springer et al., 1984, 1987). Common murres at St. George Island declined in number by about 30 percent between 1976 and 1987, but have recovered by about 12 percent since then (Dragoo and Sundeth, 1993). They declined by about 70 percent on St. Paul Island between 1976 and 1988. No trend is apparent at either Nunivak Island or Cape Peirce. Common murres apparently declined at Bluff between 1975 and the early 1980s, but numbers have been stable since that time. Abundance of common murres on Agattu Island has nearly doubled since the mid-1970s. Thick-billed murres decreased by about 30 percent on the Pribilof Islands since the mid-1970s, although numbers on both islands have been relatively constant since the mid-late 1980s. They have increased by 300 to 400 percent on Buldir Island in the past 15 years. Estimates of total murre abundance in four colonies in the eastern Aleutians in periods sampled between the early 1970s and late 1980s (Bailey and Trapp, 1986; O'Daniel et al., 1990), while inconclusive, indicate possible declines of 30 to 90 percent. The abundance of murres (predominantly thick-billed) on St. Lawrence Island apparently did not change overall in the 

BIOLOGY OF HIGHER TROPHIC LEVELS 123 interval 1972 to 1981 (Roseneau et al., 1985), but it might have increased somewhat since then (Piatt et al., 1988). Numbers of murres apparently have declined by 25 to 60 percent at several inshore colonies in the western Gulf of Alaska for reasons that predate the oil spill of the Exxon Valdez (Piatt, 1994). The pattern is different at two offshore colonies, Middleton Island and the Semidi Islands. Numbers of murres at both locations appear to have fluctuated since the mid-1970s, but there is no indication of consistent change during that time (Dragoo and Bain, 1990; Gould et al., 1984; S. Hatch, unpublished data). Between the mid-1950s and mid-1970s, however, murres increased by about an order of magnitude on Middleton Island. The increase, like that of kittiwakes on Middleton Island, may have resulted from the creation of nesting habitat by the 1964 earthquake. One of the longest records of murre abundance in Alaska is from Cape Thompson, in the eastern Chukchi Sea, where Swartz (1966) took a through census of the birds in 1960–61. Since then murres have steadily declined by about 50 percent overall. In contrast, murres have been gradually increasing nearby at Cape Lisburne, at least since the mid-1970s. Introduced Mammals Introduced mammals have devastated seabird populations throughout the Aleutian Islands and on many islands in the Gulf of Alaska (Bailey, 1990; Bailey and Kaiser, 1993; Murie, 1959). As long ago as 1750 and peaking in the early years of this century, foxes were released on islands where they were raised for the fur trade. The abundant natural food (birds) and the escape-proof nature of islands made them ideal location for raising foxes. Foxes caused the greatest damage, but microtine rodents and ground squirrels, which were released on numerous islands as additional sources of food for the foxes, added to the problem by preying on eggs and chicks that were inaccessible to foxes. Hardest hit were ground-nesting species, particularly Leach's and fork-tailed storm petrels, ancient murrelets, Cassin's auklets, crested auklets, tufted puffins, Canada geese, ptarmigan, passerines, and various species of ducks. Rats have long been a threat to seabirds in Alaska. Increased shipping from new ports on the Pribilofs is a cause for concern, as evidenced by the sighting in 1992 of a rat on a mooring rope of a ship docked at St. Paul Island (A. Sowls, personal communication). Rats have wiped out six species of seabirds on Langara Island (Bailey and Kaiser, 1993; Bertram, 1989), which lies off the northern coast of the Queen Charlotte Islands, British Columbia. Rats escaped onto Kiska Island in the western Aleutians during World War II. The recent removal of foxes may be responsible for the marked increase in rats that now threatens the enormous colony of least auklets more than the foxes did (V. Byrd, personal communication). At present, it appears to be virtually impossible to eliminate rats from large islands such as Kiska. Gill Net Mortality Mortality of seabirds in salmon gill nets in the North Pacific was a major concern for many years (Ainley et al., 1981; DeGange and Day, 1991; DeGange and Newby, 1980; 

BIOLOGY OF HIGHER TROPHIC LEVELS 124 DeGange et al., 1985, 1992; Jones and DeGange, 1988; King et al., 1979). Japanese high-seas and land-based salmon fisheries operated in the western North Pacific south of the Aleutian Islands and in the western Bering Sea since 1952. Estimates of the total annual loss of seabirds were as high as 700,000 in the early 1970s and 450,000 in the mid-1970s. Mortality in the offshore component of the land-based fishery declined from about 150,000 in 1977 to 57,000 in 1987 because of a reduction in fishing effort. Seabirds killed in gill nets included birds from the Bering Sea and probably the Sea of Okhotsk, as well as shearwaters from the southern hemisphere. Of particular concern to the United States was the potential loss of seabirds from the western Aleutian Islands, which lie near the center of the region occupied by the Japanese mothership fishery. This fishery killed on the order of 95,000 to 250,000 seabirds annually in the early 1980s, approximately 80 percent of which were tufted puffins. Drift net fishing in U.S. waters was banned in 1988. Recent increases in puffin populations cannot be ascribed with certainty to the ban on gill net fishing in U.S. waters (Byrd et al., 1992). The number of nesting puffins on Agattu Island and Nizki-Alaid Island has increased since the mid-1970s, but not on nearby Buldir Island. The increases on Agattu Island and Nizki-Alaid Island followed not only the ban on gill nets, but also the removal of foxes from the islands in 1976 and 1977. Foxes were never introduced to Buldir Island. Therefore, it is difficult to distinguish between the effects of fishing and those of foxes on the Near Islands, and an increase on Buldir might be only now beginning (puffins do not recruit to the breeding population until the age of three to five). Consumption of Plastic Particles Several species of seabirds consume large numbers of plastic particles that they apparently mistake for prey. Plastic has been found in the stomachs of 50 species of marine birds around the world, of which the procellariids, phalaropes, and certain alcids—primarily Cassin's auklets, parakeet auklets, and puffins—are the most contaminated (Day, 1980; Day et al., 1985; Hatch, 1993; J. Piatt, unpublished data). Plastic pollution of the oceans apparently began in the 1960s and has been increasing since, with a corresponding increase in the consumption of plastics by birds. Plastic particles in the North Pacific apparently originate in the west and are carried eastward in the Subarctic and Kuroshio currents (Day and Shaw, 1987; Day et al., 1990). There is some evidence for short-tailed shearwaters and tufted puffins that particles accumulated during summer might be eliminated during winter (Day et al., 1985). Numerous effects of plastic particles on seabirds, including starvation, intestinal blockage, and ulceration, have been documented but there is little evidence that plastic consumption is detrimental to species productivity or survival. Oiling Approximately 30,000 carcasses of oiled seabirds were recovered following the grounding of the Exxon Valdez, of which about 22,000 were murres, mainly common murres (Piatt et al., 1990). Surveys at selected colonies hit by oil indicated that possibly as many as 120,000 to 

BIOLOGY OF HIGHER TROPHIC LEVELS 125 140,000 adult murres, or 60 to 70 percent of the breeding birds, were killed at those colonies (Nysewander and Dipple, 1992). A reevaluation of the data indicates that the total mortality probably was about 240,000 seabirds, including about 180,000 murres (Piatt, 1994). Piatt (1994) further argues that murre populations were in decline in the Gulf of Alaska well before the oil spill and the recent declines must be viewed in a broader context. Hunting Four species or subspecies of geese nest along the coast of the Bering Sea, particularly on the Yukon- Kuskokwim delta: greater white-fronted geese, emperor geese, cackling Canada geese, and black brant. During the 1960s and 1970s, numbers of all declined precipitously (Raveling, 1984). Restrictions on hunting during the spring subsistence harvest and during winter on the west coast of North America and in Mexico led to appreciable recoveries. However, dramatic declines in numbers of brant nesting on the Yukon-Kuskokwim delta continued into the 1980s (Sedinger et al., 1993), raising fears that management actions were not effective or that other factors were operating on the population. Sedinger et al. (1993) have suggested that continued subsistence harvest together with heavy predation on nesting birds likely explains the recent decline. The abundance of emperor geese has apparently recovered only slightly from its low point in the mid-1980s, and is still only about half as great as in the 1960s (U.S. Fish and Wildlife Service, 1989). The major difference between emperor geese and the other species is that the majority of the population winters in the Bering Sea and on the south side of the Alaska Peninsula. They were not subjected to heavy hunting pressure on the wintering grounds, and thus must be influenced more by other factors in winter that increase mortality, or by factors such as the summer subsistence harvest, which likely compounds the effects of winter mortality (Schmutz et al., 1994). Most species of juvenile geese, including emperor geese, suffer high post-fledging mortality. Mortality during winter is high for emperor geese also (C. Dau, personal communication). It is possible that winter mortality has increased in recent years, or that management of the subsistence harvest has not been effective in curtailing the take to the point that the species has been able to recover to acceptable levels. Numerous species of sea ducks also nest on the Yukon-Kuskokwim delta. Prominent among these are spectacled eiders and Steller's eider. Steller's eiders have not nested on the delta since 1975, whereas as many as 3,500 pairs might have nested there during the 1950s and 1960s (Kertell, 1991). Steller's eider is presently a candidate for threatened or endangered status under the Endangered Species Act (Quakenbush and Cochrane, 1993). Spectacled eiders have declined about 14 percent per year since the early 1970s, from an estimated historical population size of more than 47,000 pairs to fewer than 2,000 pairs today (Stehn et al., 1993). The spectacled eider was declared a threatened species in 1993. As a group, the sea ducks, like emperor geese, are very K-selected, which makes populations highly susceptible to adult mortality (Goudie et al., 1994). Thus, speculation about the cause of the declines has focused on effects of subsistence harvests, predation, and other sources of adult mortality in summer and winter (Kertell, 1991; Stehn et al., 1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 126 Sport hunting for eiders is not considered to be important, as it is for other ducks that migrate to wintering grounds south of Alaska. However, the role of the subsistence harvest is thought by some to be particularly important (e.g., Goudie et al., 1994). Alternatively, predation rates on nesting eiders might have risen as populations of geese and ducks on the Yukon-Kuskokwim delta fell during the 1960s and 1970s; predator (primarily arctic fox) numbers could have remained the same but inflicted proportionally greater losses on all species as the total number of potential prey declined. Lead poisoning has recently been identified as another possible source of adult mortality in summer. In 1992 and 1993, two spectacled eiders and one common eider were found dead or dying on the Yukon- Kuskokwim delta. All of the birds had high levels of lead in their livers and two of them had several pieces of lead shot in their digestive tracts. The presence of lead shot, the elevated lead levels in livers, and the poor body condition of the birds indicated that lead poisoning was at fault (U.S. Fish and Wildlife Service, unpublished data). Mortality during winter in the Bering Sea is also a possible factor, although very little is known about this. The wintering area of the spectacled eider is still obscure, but is probably in the western Bering Sea south of the seasonal sea ice and in polynyas south of St. Lawrence Island. Steller's eiders winter throughout the Aleutian Islands and Alaska Peninsula. The diets of both species include crustaceans and bivalves; whether these organisms have changed in abundance sufficiently to cause declines in eider populations is not known. In addition to the eiders, four other species of sea ducks that nest inland in Alaska and winter along the coast of the Gulf of Alaska and Pacific Northwest have also declined considerably in the past 30 years (Hodges et al., 1994). Surf scoters (Melanitta perspicillata ), white-winged scoters (M. fusca), and black scoters (M. nigra) declined in aggregate an estimated 33 percent between 1957 and 1992, while oldsquaws (Clangula hyemalis) declined 67 percent between 1977 and 1992. The reason for the declines is not known. MARINE MAMMALS Life History and Distribution The marine mammal fauna of the Bering Sea is particularly rich because it includes north temperate, subarctic, and arctic species (Table 4.7). Several species of the North Pacific fauna (e.g., harbor seal, Steller sea lion, sea otter, beluga whales, and Dall's porpoise) are resident in the area throughout the year. Other species (e.g., gray, fin, blue, and humpback whales) migrate into the Bering Sea during summer months to feed. Marine mammals occur in all types of habitats, including deep oceanic waters, the continental slope, and the continental shelf (Table 4.8). The majority of species are found mostly over the continental shelf and in coastal waters. Ice- associated species (e.g., polar bears, walruses, ringed and bearded seals, and bowhead whales) are found in the Bering Sea mostly during the fall and winter in association with seasonal sea ice. Ice plays a particularly significant role in the ecology of marine mammals, as it provides habitat for some species while serving as a barrier to others (Fay, 1974). Ice-associated species are not found in the Gulf of Alaska, but otherwise the fauna is similar to that of the Bering Sea (Calkins, 1986). 

BIOLOGY OF HIGHER TROPHIC LEVELS 127 Table 4.7 Marine mammal species in the Bering Sea Common Name Scientific Name Abundance/Trenda Statusb Baleen whales Gray whale Eschrichtius robustus Moderate/increasing Recovered Fin whale Balaenoptera physalus Low/unknown Endangered Minke whale Balaenoptera acutorostrata Low/unknown Unknown Blue whale Balaenoptera musculus Low/unknown Endangered Sei whale Balaenoptera borealis Low/unknown Endangered Humpback whale Megaptera novaeangliae Low/unknown Endangered Right whale Balaena glacialis Low/unknown Endangered Bowhead whale Balaena mysticetus Low/increasing Endangered Toothed whales and dolphins Sperm whale Physeter macrocephalus Moderate/unknown Endangered Cuvier's beaked whale Ziphius cavirostris Low/unknown Unknown Baird's beaked whale Berardius bairdi Low/unknown Unknown Stejneger's beaked whale Mesoplodon stejnegeri Low/unknown Unknown Beluga whale Delphinapterus leucas Moderate/stable OSP Killer whale Orcinus orca Low/unknown Unknown Dall's porpoise Phocoenoides dalli Moderate/unknown Unknown Harbor porpoise Phocoena phocoena Low/unknown Unknown Pinnipeds Northern fur seal Callorhinus ursinus High/stable Depleted Steller sea lion Eumetopias jubatus Moderate/declining Threatened Pacific walrus Odobenus rosmarus divergens High/stable OSP Harbor seal Phoca vitulina richardsi Moderate/declining Unknown Spotted seal P. largha High/unknown Unknown Ribbon seal P. fasciata Moderate/unknown Unknown Ringed seal P. hispida High/unknown Unknown Bearded seal Erignathus barbatus High/unknown Unknown Others Polar bear Ursus maritimus Low/stable OSP Sea otter Enhydra lutris Moderate/stable OSP aLow = less than 10,000; moderate = 10,000–100,000; high = more than 100,000. bEndangered and threatened refer to Endangered Species Act listings. OSP means within the optimum sustainable population range as defined by the Marine Mammal Protection Act. Depleted means below the OSP range. Source: Based on Lowry and Frost (1985). 

BIOLOGY OF HIGHER TROPHIC LEVELS 128 Table 4.8 General oceanographic/habitat associations of Bering Sea Marine mammals Oceanic/Deep Water Continental Slope/ Slope Break Continental Shelf/ Coastal Waters Sei whale Fin whale Gray whale Right whale Minke whale Humpback whale Sperm whale Blue whale Minke whale Cuivier's beaked whale Dall's porpoise Bowhead whale Baird's beaked whale Stejneger's beaked whale Beluga Steller sea lion Killer whale Ribbon seal Harbor porpoise Pacific walrus Northern fur seal Steller sea lion Harbon seal Spotted seal Ringed seal Ribbon seal Bearded seal Polar bear Sea otter Source: Based on Lowry et al. (1982). Information on the distribution and abundance of Bering Sea marine mammals is incomplete (see review in Lowry et al., 1982). For most species, seasonal distribution is known only in general terms and winter distributions are poorly understood. Available estimates of population sizes are generally imprecise, and many of them are out of date. The abundance of most whales and dolphins is low, and species such as right and blue whales are (Table 4.7). Bowhead and gray whales are increasing in numbers. Beluga whale abundance is probably stable, and the trend in abundance of all other cetaceans is unknown. Seven species of large whales are classified as endangered under provisions of the Endangered Species Act. Pinnipeds are generally more abundant than cetaceans with the population size of several species estimated to number over 100,000. Steller sea lions are classified as threatened under the Endangered Species Act, and northern fur seals on the Pribilof Islands are listed as depleted under provisions of the Marine Mammal Protection Act. Bering Sea marine mammals prey on a wide array of species and feed at several different trophic levels (Frost and Lowry, 1981a; Lowry et al., 1982). Most phocid seals, fur seals, and sea lions feed principally on fishes, with invertebrates making up a relatively small part of the diet (Table 4.9). Bearded seals and walruses eat mostly epifaunal and infaunal invertebrates, and thus their diets differ greatly from other pinnipeds. Toothed whales feed principally on fishes 

BIOLOGY OF HIGHER TROPHIC LEVELS 129 Table 4.9 Relative importance of major prey types in the diets of pinnipeds in the Bering Sea Species Pelagic and Demersal Pelagic Nekto- Epifaunal Infaunal Semidemersal Fishes Nektonik benthonic benthic benthic Fishes Invertebrates Invertebrates Invertebrates Invertebrates Harbor Major Minor --- Minor --- --- seal Spotted Major Minor Majora Major --- --- seal Ribbon Major Major --- Minor --- --- seal Ringed Major Minor Major Major --- --- seal Bearded Minor Minor --- Major Major Major seal Walrus --- --- --- Minor Minor Major Fur seal Major Minor Major --- --- --- Sea lion Major Major Minor --- --- --- aFor juveniles Source: Based on Frost and Lowry (1981a). Table 4.10 Relative importance of major prey types in the diet of cetaceans in the Bering Sea Species Pelagic and Demersal Octopus Copepods Euphausiids Nekto- Epifaunal Marine Semidemersal Fishes and benthonic Invertebrates Mammals Fishes Squids Invertebrates Right --- --- --- Major Minor --- --- --- whale Bowhead --- --- --- Major Major Minor --- --- whale Blue Minor --- Minor Minor Major --- --- --- whale Fin Major --- Minor Major Major --- --- --- whale Sei Minor --- Minor Major Minor --- --- --- whale Minke Major --- Minor Minor Major --- --- --- whale Gray Minor --- Minor --- --- Major Major --- whale Sperm Minor Major --- --- --- --- Minor --- whale Beaked Minor Major Major --- --- Minor --- --- whale Killer Major Minor Major --- --- --- --- Major whale Beluga Major Minor Minor --- --- Minor --- --- whale Harbor Major --- Minor --- --- Minor --- --- porpoise Dall's Minor Major Major --- Minor Minor --- --- porpoise Source: Based on Frost and Lowry (1981a) and Lowry et al. (1982). 

BIOLOGY OF HIGHER TROPHIC LEVELS 130 and cephalopods, whereas most baleen whales eat planktonic crustaceans and small schooling fishes (Table 4.10). Important exceptions to this pattern are killer whales, which commonly eat other marine mammals, and gray whales, which feed mostly on epibenthos. Sea otters eat primarily benthic invertebrates, whereas polar bears consume mainly phocid seals. The biology and population dynamics of Bering Sea marine mammals have been reviewed by Lowry and others (1982). Calkins (1986) reviewed information on marine mammals in the Gulf of Alaska. Summaries are provided here for species of concern in the Bering Sea because they have shown unexplained population declines. Similar information is presented for some of the large whales, because the large reduction in the abundance of these species could have contributed to changes in the ecosystem that are of concern today. Steller Sea Lion Steller sea lions inhabit waters of the North Pacific rim from California through the Aleutian Islands to Japan (Loughlin et al., 1984). They pup and breed in June and July in rookeries on relatively remote islands, rocks, and reefs. Sea lions disperse widely during the nonbreeding season, and marked animals have been seen far from the locations where they were tagged (NMFS, 1992). There is some evidence, however, that females generally return to rookeries where they were born to give birth and mate (Calkins and Pitcher, 1982; Loughlin et al., 1984). Recent genetics studies suggest that there are two relatively well-differentiated populations, one of animals inhabiting the region from Oregon through southeast Alaska, and the other of those in the region from the northern Gulf of Alaska through the Aleutian and Komandorsky island (Bickham et al., in press). In the Bering Sea and Gulf of Alaska, sea lions eat a variety of fishes and cephalopods (Calkins and Goodwin, 1988; Lowry et al., 1982; Merrick and Calkins, in press). Walleye pollock are an important food (Lowry et al., 1989). Small pollock (those less than 20 cm) appear to be more commonly eaten by juvenile sea lions than by older animals (Merrick and Calkins, in press). Table 4.11 provides information on sea lion diets. Sea lion rookeries and haulout sites are widely distributed, from British Columbia and southeast Alaska, throughout the Aleutians to the Sea of Okhotsk. In the late 1950s and early 1960s, Steller sea lions were abundant, with the total population in the North Pacific estimated to be about 240,000 to 300,000 (Kenyon and Rice, 1961). However, these early sea lion surveys were conducted in conjunction with sea otter surveys over a period of several years during various months of the year. Although the estimate produced by Kenyon and Rice provides some indication of sea lion abundance at that time, there is general agreement that these early surveys are not directly comparable to those conducted from the 1970s to the present. Recent efforts have attempted to maximize the number of animals counted by conducting surveys at midday during the peak of the pupping season (Braham et al., 1980; Loughlin et al., 1992; Merrick et al., 1987). Sea lion counts (Table 4.12) are not estimates of total population size, but rather minimum estimates of the number of animals using a site or group of sites (Loughlin et al., 1984, 1992; NMFS, 1992). Loughlin and others (1984) conducted the first comprehensive review of population trends in Steller sea lions between 1956 and 1980. They found evidence for an increase in numbers 

BIOLOGY OF HIGHER TROPHIC LEVELS 131 Table 4.11 Geographic and temporal distribution of samples used to determine the composition of Steller sea lion dietsa. AREA N DATE MAJOR PREY SOURCE Western Bering Sea 86 1981 Pollock Calkins, cited in Lowry et al., 1989 Bering Sea/Aleutians 2 1949–51 Wilke and Kenyon, 1952 1958–63 Ficus and Baines, 1966 10 1976 4 1990–91 Lowry et al., 1982 16 1945–46 Atka mackerel Merrick et al., 1993 3 1958 Gulf of Alaska 7 Imler and Sarber, 1947 11 1959 Smelt, greenling, Mathinsen et al., 1962 4 cephalopods 1958–63 56 Cephalopods, sand lance, rockfish Thorsteinson and Lensink, 1962 6 1985–86 Fiscus and Baines, 1966 1945–46 15 Pollock, squid, herring Calkins and Goodwin, 1988 Southeast Alaska 8 Imler and Sarber, 1947 2 Fiscus and Baines, 1966 14 Pollock Calkins and Goodwin, 1988 aMajor prey are listed only for samples of 15 or greater. Source: Committee on the Bering Sea Ecosystem. Table 4.12 Counts of adult and juvenile Steller sea lions at rookery and haulout sites in seven subareas of Alaska during June–July, 1975–92 Gulf of Alaska Aleutian Islands Year Southeast Alaska Eastern Central Western Eastern Central Western 1975 19,769 1976 7,053 24,678 8,311 19,743 1977 19,195 1979 6,376 36,632 14,011 1982 6,898 1985 19,002 6,275 7,505 23,042 1989 8,471 7,241 8,552 3,908 3,032 7,752 1990 7,629 5,444 7,050 3,915 3,801 7,988 2,327 1991 7,715 4,596 6,273 3,734 4,231 7,499 2,411 1992 7,558 3,738 5,721 3,720 4,839 6,399 2,869 Change 1975/79–1992 +19% -47% -77% -55% -76% -83% -80% Source: Sease et al. (1993). 

BIOLOGY OF HIGHER TROPHIC LEVELS 132 in the central and western Aleutians, but for a large decrease in the eastern Aleutians, confirming the results of Braham et al. (1980). Loughlin et al. (1984) reported that both increases and decreases were evident in the Gulf of Alaska. The number of sea lions counted in surveys of the Kenai Peninsula to Kiska Island (i.e., the central and western Gulf of Alaska and the eastern and central Aleutian Islands) between 1985 and 1989 declined by 63 percent (Loughlin et al., 1990). In 1989, the range-wide population estimate of 116,000 was only about 39 to 48 percent of that estimated 30 years before (Loughlin et al., 1992). This documented decline resulted in a December 1990 listing of Steller sea lions as threatened under provisions of the Endangered Species Act (NMFS, 1992). Based on these surveys, it appears that the numbers of sea lions initially began to decline in the eastern Aleutians and that this decline likely began by the early 1970s. A decline in counts of adult and juvenile sea lions had become apparent in the central Gulf of Alaska by the late 1970s and in the western Gulf of Alaska and the central Aleutians perhaps a few years later, by the early 1980s (Byrd, 1989; Merrick et al., 1987; NMFS, 1992; Trites and Larkin, 1992). Counts at rookeries in the central and western Aleutians showed considerable variation, but clear evidence of decline since the mid-1980s. Counts of pups confirmed that a major population decline occurred in this region (Sease et al., 1993). Although some authors differ regarding when these declines began, all agree the declines began later in the Gulf of Alaska and western and central Aleutians than in the eastern Aleutians. In Russia, the situation is similar to that in the eastern Bering Sea and Gulf of Alaska, with the present abundance of sea lions much reduced from historical levels. According to Perlov (1991), in 1988–89 there were 13,800 to 16,300 animals counted in Kamchatka, the Kuril Islands, and the Okhotsk Sea, compared to 42,500 to 52,300 in the 1970s. Counts made in summer 1994 indicate that sea lion numbers have continued to decline in Kamchatka and the Kuril Islands. In the Komandorsky Islands, the number of animals breeding at the Medney Island rookery appears to be stable, but overall numbers have declined since 1989 (V. Burkanov, personal communication). In contrast to the pattern of declining counts elsewhere, counts in the eastern Gulf of Alaska and southeast Alaska have been stable or increasing over the past two decades (NMFS, 1992; Trites and Larkin, 1992). Similarly, the number of Steller sea lions (both pups and older animals) in British Columbia has increased at about 2.5 percent per year between the early 1970s and 1992 (P. Olesiuk, personal communication). There is little information on fluctuations in Steller sea lion numbers that may have occurred before 1960. Fluctuations in numbers that have been documented at the Pribilofs and in British Columbia and Oregon before the mid-1960s have all been explained as due to direct human exploitation (Bigg, 1985; Kenyon and Rice, 1961; Lyman, 1988). According to Kenyon (1962), Steller sea lions were very abundant in the Pribilof Islands when the islands were discovered in 1786, but they were soon overhunted. When they were afforded a measure of protection, numbers grew from a few hundred in 1914 to about 6,000 in 1960 (Kenyon, 1962). Bigg (1985) speculated that the number of animals in British Columbia may have been depressed in the early 1800s by the native hunt for meat and other products. Numbers were thought to have increased in the late 1800s when the level of native hunting was reduced. Sea lion pup production increased at a rate of 6.8 percent per year at Forrester Island, British Columbia, during 1961–73, a period when animals there were not exploited (Bigg, 1985). 

BIOLOGY OF HIGHER TROPHIC LEVELS 133 Northern Fur Seal Northern fur seals breed on a few major rookeries in the North Pacific Ocean and range widely at sea during the nonbreeding season. Five stocks have been identified that breed on six island groups: (1) Komandorsky Islands, (2) Kuril Islands, (3) Robben Island, (4) Pribilof Islands and Bogoslof Island, and (5) San Miguel Island (NMFS, 1993a). Adults belonging to these stocks are for the most part geographically separated during the breeding season, but some interchange does occur. Rookeries on St. Paul and St. George islands in the Pribilof Islands account for over 70 percent of the world population. A number of studies have been conducted on the diets of northern fur seals, beginning with the work of Lucas (1899). However, the most extensive study of northern fur seal diets is based on the pelagic sampling of over 18,000 fur seals between 1958 and 1974 (reanalyzed by Perez and Bigg, 1986). Of the fur seal stomachs collected, 7,373 contained food and an additional 3,326 had trace remains of food. These data showed marked seasonal and geographic variation in the species consumed. In the eastern Bering Sea, pollock, squid, and capelin accounted for about 70 percent of the energy intake by fur seals (Perez and Bigg, 1986). In contrast, sand lance, capelin, and herring were the most important prey in the Gulf of Alaska (Table 4.13). Since 1974, only three relatively small samples have been taken (in 1981, 1982, and 1985) to investigate fur seal diets. Analysis of these data showed that pollock and squid were the most frequently eaten prey in the eastern Bering Sea, and that there was a positive correlation between pollock year-class strength and the frequency of pollock in fur seal diets (Sinclair et al., 1994). No date are available for either region since 1985. The abundance of northern fur seals has fluctuated greatly over the past 200 years, largely due to commercial harvesting (NMFS, 1993a). Excessive harvests reduced the number of fur seals in the Pribilof Islands, from an estimated 3 million animals in the 1867 to only 200,000 to 300,000 by 1910 (Kenyon et al., 1954; Lander and Kajimura, 1982). By the 1940s, the Pribilof population had recovered substantially, but, as the estimated number of seals approached 1.5 million, the growth rate of the population was reduced. Between 1956 and 1968, 315,000 male fur seals were killed in an attempt to increase productivity, and thus increase the size of commercial harvest (Chapman, 1961; Lander, 1980). The expected increase in productivity did not occur. Rather pup production on St. Paul Island declined by 7 percent per year from 1975 to 1983, and that on St. George Island declined by 6 percent per year from 1973 to 1990 (York, 1990). The size of the Pribilof Islands population peaked in about 1950 at over 2 million animals, but it has declined by over 50 percent since then (Table 4.14). The Pribilof Islands stock of fur seals was declared depleted under provisions of the Marine Mammal Protection Act in June 1988 (NMFS, 1993a). Fur seal numbers on the Komandorsky Islands, Kuril Islands, and Robben Island (in the Sea of Okhotsk) were greatly reduced by the early 1900s (Lander and Kajimura, 1982). They increased in these areas through the mid-1960s (Vladimirov, 1991). By the late 1960s, pup production at Robben Island had begun to decline, and the decline has continued to the present (Yoshida and Baba, 1982). In 1989–90, the estimated Robben Island population of 60,000 was only about one-third as large as its maximum in 1967 (190,000) (Vladimirov, 1991). In contrast seal populations in the Komandorsky and Kuril islands have been comparatively stable. In 1988–1990 the Kormandorsky Island population numbered 225,000 to 230,000, only slightly less than 

BIOLOGY OF HIGHER TROPHIC LEVELS 134 Table 4.13 Geographic and temporal distribution of samples used to determine the composition of northern fur seal dietsa Area n Year Major Prey Source Bering Sea 373 <1900 Pollock, squid Lucas, 1899 1749 1958–74 Pollock, squid, capelin Perez and Bigg, 1986 73 1981, 1982, 1985 Pollock, squid Sinclair et al., 1993 Aleutians 309 1958–74 Sand lance, capelin, mackerel Perez and Bigg, 1986 North Pacific 562 1958–74 Herring, anchovy, squid Perez and Bigg, 1986 Gulf of Alaska 38 <1900 Rockfishes Alexander, 1892 36 <1900 Squids, rockfishes Lucas, 1899 12 1930s May, 1937 104 1950–51 Herring Wilke and Kenyon, 1952 1163 1958–74 Sand lance, capelin, herring Perez and Bigg, 1986 a Major prey are listed only for samples of 15 or greater. 

BIOLOGY OF HIGHER TROPHIC LEVELS 135 its maximum of 255,000 in the late 1970s. In the Kuril Islands, the 1988 population estimate of 45,000 to 50,000 was about 20 percent lower than the 1977–78 peak of 60,000 (Vladimirov, 1991). Table 4.14 Estimates of population abundance and pup production for northern fur seals on the Pribilof Islands Year(s) Stock size Number of pups born 1949–1951 2,100,000 531,000 1970 1,200,000 306,000 1974 1,250,000 326,000 1983 877,000 198,000 1990 1,012,000 253,000 Source: NMFS (1993a). With respect to newly colonized areas, northern fur seal pups were first born on San Miguel Island in 1968, and pup production increased to over 1,000 in 1982 (DeLong et al., 1991) on Bogoslof Island, pups were first noted in 1980 (Lloyd et al., 1981), and production has increased to more than 500 pups born in 1993 (NMFS, unpublished data). Because they have been heavily exploited, there is little understanding of the frequency or magnitude of natural fluctuations in northern fur seal populations. When the Pribilof Islands population was recovering the overexploitation in the first half of this century, increased at about 8 percent per year, despite limited commercial harvests (NMFS, 1993a). By contrast previously depleted but currently unexploited stocks of antarctic (Arctocephalus gazella) and subantarctic (A. tropicalis) fur seals have been increasing at rates of about 15 percent per year (Croxall and Gentry, 1987). There is no information that can be used to estimate the likely rates of natural declines. Harbor Seal Harbor seals occur in coastal waters of the North Pacific from Baja California through the Aleutian Islands to Japan. Within this broad range there may be two subspecies, Phoca vitulina richardsi in western North America and P. v. stejnegeri in eastern Asia (Shaughnessy and Fay, 1977). In the Bering Sea, harbor seals occur mostly south of areas affected by seasonal sea ice. To the north, they are replaced by a closely related species, the spotted seal. 

BIOLOGY OF HIGHER TROPHIC LEVELS 136 There is relatively little known about the foods of harbor seals in the Bering Sea (Lowry et al., 1982), however, the existing data are summarized in Table 4.15. Abundance estimates of harbor seals in Alaska consist, for the most part, of single counts made at individual haulout sites (Hoover, 1988b). Surveys designed to estimate regional abundances and trends were begun in the mid-1970s, and counts have been made in Bristol Bay at intervals since then (Table 4.16). At sites along the Alaska Peninsula, recent counts are lower than in the mid-1970s, but if the high counts from 1975 and 1976 are discounted, the decline has not been dramatic. In contrast, it appears that the number of harbor seals using Nanvak Bay has decreased by more than 80 percent. Harbor seal numbers have also declined dramatically in the Gulf of Alaska at Tugidak Island and in Prince William Sound. At Tugidak Island, counts dropped by about 85 percent between 1976 and 1988 (Pitcher, 1990). In Prince William Sound, harbor seals have declined by an estimated 57 percent between 1984 and 1992 (Frost and Lowry, 1994). In southeast Alaska, seal numbers have been relatively stable since 1984 (J. Lewis, personal communication; Loughlin, 1994). Long-term records of harbor seal abundance in the North Pacific are not available. Heavy hunting pressure in the mid-1900s, often associated with bounty programs, very likely resulted in reduced harbor seal populations in some areas. Since harbor seals in British Columbia were protected from hunting in 1970, the population has grown at an average rate of about 12.5 percent per year (Olesiuk et al., 1990). In recent years, the numbers of harbor seals and California sea lions (Zalophus californianus) have increased greatly in California, Oregon, and Washington (Boveng, 1988a, 1988b). Baleen Whales With the exception of the bowhead, all large whales of the Bering Sea and Gulf of Alaska are summer seasonal residents (Lowry et al. 1982). They winter in temperate waters of the North Pacific and migrate north to feed in summer. Feeding grounds correspond to locations where prey of the appropriate type are concentrated. For example, gray whales are often found in the northern Bering and Chukchi seas where the benthic infauna are particularly abundant (Highsmith and Coyle, 1992; Johnson and Nelson, 1984). A large number of blue, fin, sei, and humpback whales have been found in comparatively small areas with high concentrations of primary and secondary productivity (e.g., Nemoto, 1963). Currently, bowhead whales leave the Bering Sea in the summer and go to the eastern Beaufort Sea, where they apparently do most of their feeding (Lowry, 1993). However, before their decimation by commercial whalers, some bowheads spent the summer, and presumably fed, in the Bering and Chukchi seas. Available data on the prey of baleen whales in the Bering Sea were reviewed in Frost and Lowry (1981a) and Lowry et al., (1982). In general, descriptions of diets come from studies conducted in conjunction with commercial whale harvests, and they may or may not reflect recent diets. Gray whales are unique in that they feed principally on several species of benthic gammarid amphipods. Right whales appear to have the most specialized feeding strategy. Studies conducted in the North Atlantic suggest that right whales require high densities of copepods concentrated in surface waters for effective feeding (Kenney et al., 1986; Mayo and Marx, 1990). Sei whales eat copepods and euphausiids, while blue whales eat primarily 

BIOLOGY OF HIGHER TROPHIC LEVELS 137 Table 4.15 Geographic and temporal distribution of samples used to determine the composition of harbor seal dietsa Area n Year Major Prey Source Bering Sea 6 1973 Lowry et al., 1979 8 1979 Lowry et al., 1982 19 1981 Sand lance, Smelt, sculpins Lowry et al., 1982 20 1985 Herring, capelin L.F. Lowry, unpubl. data 7 1954 Wilke, 1957 11 1959–62 Kenyon, 1965 17 1968–73 Shrimp, mysids, octopus Burns and Gol'tsev, 1984 Gulf of Alaska 3 1972 Lowry et al., 1979 67 1945–46 Eulachon Imler and Sarber, 1947 269 1973–78 Pollock, octopus, capelin Pitcher, 1980 99 1945–46 Pollock, herring, flatfishes Imler and Sarber, 1945 a Major prey are listed only for samples of 15 or greater. 

BIOLOGY OF HIGHER TROPHIC LEVELS 138 Table 4.16 Counts of harbor seals in Bristol Bay Year North Side of Alaska Peninsulaa Nunivak Bayb 1975 17,245 2,918 1976 23,805 --- 1977 12,584 --- 1979 --- 2,000 1981 --- 3,100 1983 --- 2,500 1985 11,728 --- 1990 10,105 470 1991 10,192 400 aSum of maximum counts at each of four haulouts made in June. bMaximum count made in August-September. Source: Sease (1992). 

BIOLOGY OF HIGHER TROPHIC LEVELS 139 euphausiids. Fin whales, humpback whales, and minke whales have a more diverse diet, eating euphausiids as well as schooling fishes such as capelin, herring, and pollock. Estimates of stock sizes of baleen whales (Table 4.17) refer to North Pacific (or eastern North Pacific) populations and do not represent the actual number of animals using the Bering Sea and Gulf of Alaska regions. Nonetheless, it is clear that baleen whales were once numerous in these regions, and with the exception of gray whales, their populations are now much smaller. Reliable estimates of the absolute former abundance of most species in the Bering Sea and Gulf of Alaska are lacking, but a sense of their initial stock sizes can be inferred from the numbers harvested. For example, between 1955 (when fin whales began to be heavily harvested in the Bering Sea) and 1970 (when they were rare) about 11,000 whales were killed. Between 1960 and 1967, an additional 4,000 were killed in the northern Gulf of Alaska, which virtually eliminated the species from that region as well. During the same intervals, about 5,000 sei whales were killed in the northern Gulf of Alaska, and about 1,500 blue and 3,300 humpback whales were killed in the northern Gulf of Alaska and Aleutian islands. An even greater slaughter of sperm whales occurred during this time, with some 26,000 animals taken from the Bering Sea alone (International Whaling Commission, unpublished data; Kasuya, 1991). With the exception of gray and bowhead whales, for most species the current trend in population size in the Bering Sea and Gulf of Alaska region is uncertain. Gray whales have increased in numbers, and the current population size is about the same as that which probably existed before commercial whaling (Buckland et al., 1993). Surveys of whales in the Gulf of Alaska in 1980 indicated that populations of the other previously exploited species remained very depressed (Rice and Wolman, 1982). Although completely protected from commercial whaling since 1946, North Pacific right whales have shown no signs of recovery and are still extremely rare (Scarff, 1991). In contrast, the Bering-Chukchi-Beaufort stock of bowhead whales is now increasing, and the population may number one-half to one-third its former size (Zeh et al., 1993). DISCUSSION OF POPULATION DECLINES In the absence of significant human exploitation, the size of marine mammal populations can be expected to change over time in response to natural changes in the availability of resources and, in some cases, to changes in the physical environment. In general, marine mammal populations are thought to be food-limited (Estes, 1979), and therefore population changes are most likely to reflect changes in the amount of food available to individuals rather than a direct response to physical changes in the environment. Natural frequencies of population change will differ among different species or groups, but in marine mammals, like other large mammals, natural changes can be expected to occur on interdecadal time scales (Fowler and Smith, 1981). Pinnipeds and cetaceans are long- lived species, with delayed sexual maturity, low fecundity (i.e., single young), and high adult survival rates. These characteristics constrain the annual finite rate of increase of pinniped and cetacean populations to about 3 percent to 15 percent (Best, 1993; Cooper and Stewart, 1983; Lander and Kajimura, 1982; Olesiuk et al., 1990; Reilly and Barlow, 1986; Zwanenburg and Bowen, 1990). At these rates of increase, the potential doubling time of population size is about 5 to 23 years. 

BIOLOGY OF HIGHER TROPHIC LEVELS 140 Table 4.17 Estimates of initial and current populations of exploited North Pacific baleen whales Stock Size Species Stock Initial Current Current % of Initial Blue whale North Pacific 4,900 1,600 33 Fin whale North Pacific <45,000 16,625 <37 Sei whale North Pacific 40,000 9,110 23 Humpback whale North Pacific 15,000 <2,000 13 Right whale North Pacific No est. No est. No est. Bowhead whale Western Arctic 18,000 7,800 43 Gray whale E. North Pacific <20,000 21,113 >100 Source: NMFS (1991b). 

BIOLOGY OF HIGHER TROPHIC LEVELS 141 Although life history characteristics constrain marine mammals to low rates of population increase, the rate of population decline is not similarly constrained. Populations can decrease at rates that greatly exceed their rates of increase, even in the absence of hunting. The large and rapid reductions in harbor seal populations and several other species of marine mammals as a result of viral epizootics serve to illustrate this point (see review by Harwood and Hall, 1990). The recent mass mortality of harbor seals in Europe is particularly well documented. The first indications of this event occurred in February and March 1988, and by December of that year more than 18,000 carcasses had been reported. In the main areas affected by the virus, populations were reduced by 40 to 75 percent in less than one year (Heide-Jorgensen et al., 1992). The underlying cause of these deaths was a previously undescribed morbillivirus, now known as phocine distemper virus (Breuer et al., 1988; Kennedy et al., 1988; Osterhaus and Vedder, 1988). In the absence of a major disease event, however, marine mammal populations do not normally decline rapidly, because they have life history traits that tend to dampen the influence of factors that might negatively affect population size (Estes, 1979). For example, relatively short-term changes in climate, such as El Niño Southern Oscillation (ENSO) events, are known to have widespread effects on marine ecosystems (Trillmich and Ono, 1991). Reduction in the availability of prey resulting from ENSO events causes increased pup and juvenile mortality and reduced adult survival in some pinniped populations (Trillmich and Ono, 1991). Reduced productivity for one of two years has had relatively little overall effect, however, because of the typically high adult survival rates and the large number of age classes in the population. Few marine mammal populations have been monitored for long periods. In most cases, the longest time series have been obtained for commercially exploited species, and in cases where populations are no longer harvested, there are data only on the recovery phase (e.g., Cooper and Stewart, 1983; Zwanenburg and Bowen, 1990). As a result, there is little information on natural frequencies or amplitudes of population change. Testa and others (1991) reported quasi-cyclic patterns in three species of antarctic pinnipeds over a period of about 20 years, suggesting changes in productivity separated by four-to-six-year intervals. They speculated that these changes might be associated with large-scale oceanographic variations. Although these data point to the possibility of relatively high-frequency change in some systems, neither the rate of change nor the magnitude of the effects on population size is known. Because marine mammal population sizes fluctuate over time, can it be determined whether an observed decline is unusual and should be of concern? An unusual decline could simply be one that is encountered infrequently. In this sense, the population changes caused by recent viral epizootics in regions other than the Bering Sea would constitute unusual declines. In this and similar situations, however, the underlying causes of the declines are reasonably clear and thus they are not unusual in the sense of being unexplained changes. Some southern elephant seal populations have been declining at a rate of about 2 to 5 percent per year for periods of up to 40 years with no direct exploitation. These changes have been described as drastic, in that populations have declined by more than 50 percent in less than three generations (Hindell and Burton, 1987). By such criteria, the observed declines in the numbers of Steller sea lions, northern fur seals, and harbor seals in the Bering Sea and Gulf of Alaska have also been ''drastic." In describing these declines in this way, there is the clear implication that in light of existing knowledge, the nature of these declines is cause for concern. 

BIOLOGY OF HIGHER TROPHIC LEVELS 142 For the Bering Sea and Gulf of Alaska, it is the broad-scale, large, and sustained nature of the declines in some pinniped populations that is thought to be unusual. In part, these declines seem unusual because the same species are stable or increasing in numbers in other parts of their range in the North Pacific. Regardless of what terms are used to describe the recent declines of Bering Sea and Gulf of Alaska pinnipeds, given the lack of data on natural frequencies of population change, it will be difficult to distinguish between human-and nonhuman- induced population changes, and even more difficult to attribute causation. Declines in the number of Steller sea lions have occurred over most of the species range in the Bering Sea and west-central Gulf of Alaska, but not in the eastern Gulf of Alaska and southeastern Alaska or in British Columbia. In the case of harbor seals, the decline in numbers is well documented only in the Prince William Sound and Kodiak regions of the Gulf of Alaska, whereas numbers are clearly increasing in British Columbia. The number of fur seal pups born on St. Paul Island declined until 1983 but has been stable over the past decade, while the decline in pup production on St. George Island has continued. The number of fur seals born on Robben Island in the Sea of Okhotsk has been declining since the late 1960s, but pup production at the Komandorsky and Kuril islands has been relatively stable. For each of these species, then, understanding why numbers in some regions are declining while others are not could provide important clues about the causes of the declines. This comparative approach could be extended to ask whether species in the Bering Sea and Gulf of Alaska other than fur seals, sea lions, and harbor seals have shown similar changes in abundance. Although population trends in ice-breeding seals of the northern Bering Sea and cetaceans in the Bering Sea and Gulf of Alaska are poorly known, it is clear that not all species are declining or failing to recover from overexploitation. Gray whales, walruses, and sea otters have recovered from drastic reductions caused by hunting, and their populations now appear to be relatively stable. Bowhead whales are increasing at about the rate that would be expected for such a population. It is perhaps significant that these mammals are not linked to the pelagic food web of the Bering Sea and Gulf of Alaska. Gray whales, walruses, and sea otters feed mostly on benthic organisms, while bowhead whales feed principally in the Beaufort and Chukchi seas. On the other hand, whale populations that do not seem to be recovering rapidly from depletion (e.g., right, blue, fin, sei, and humpback) are those that feed on zooplankton and/or small fishes. However, the apparent failure of most Bering Sea and Gulf of Alaska whales to increase after hunting was stopped may be something of an artifact of poor monitoring, because there have been relatively few comprehensive and dedicated survey efforts. The few surveys that have been carried out (e.g., Brueggeman et al., 1984; Rice and Wolman, 1982), however, have not detected substantial increases. It is also possible that for some of the species harvested more recently, not enough time has elapsed for significant increases to have occurred. To the extent that significant recovery has not occurred, it appears that the Bering Sea situation is unusual. Best (1993) compiled data from severely depleted whale stocks worldwide and concluded that at least 77 percent of all monitorable stocks are either believed or known to be increasing. Included among those increasing are several stocks of right whales in the southern hemisphere, which is marked contrast to the situation for right whales in the Bering Sea and Gulf of Alaska. Although there is no good estimate of stock size for North Pacific right whales, it is clear that they are rare. Scarff (1991) stated that Japanese scouting boats operating in the North Pacific during 1965 to 1979 saw only one right whale per 14,000 miles of searching 

BIOLOGY OF HIGHER TROPHIC LEVELS 143 effort. Brueggeman et al. (1984) saw only two in more than 5,000 nautical miles of dedicated survey effort from ships and aircraft in the Bering Sea during 1982. The three species of pinnipeds that have declined in abundance feed largely on forage fishes and commercially exploited species in the northern Gulf of Alaska, Bering Sea, and Aleutian Islands. When Lowry and Frost (1985) examined the information available on population biology and feeding of Bering Sea marine mammals, they concluded that three species overlapped significantly in the foods they prey on and commercial fisheries. The species were northern fur seals, Steller sea lions, and harbor seals. Based on first principles, a population that is not subject to immigration or emigration will decline only when the number of deaths exceeds the number of births. Therefore, changes in population parameters, at least in U.S. waters, must have occurred such that fecundity has declined, mortality has increased, or both. It is therefore important to understand what parameters have changed before trying to explain what has caused the changes. Population modeling is a useful tool for examining how changes in various parameters may affect population trends. For example, York (1994) modeled the population dynamics of Steller sea lions at Marmot Island, where numbers had declined about 5 percent per year between 1975 and 1985 (Merrick et al., 1992). She concluded that a 10 to 20 percent decrease in the survival of juveniles (i.e., from birth to age three) was most consistent with the changes in demographic data observed over the period. While these results are useful for suggesting which population parameters may have changed and for estimating minimum levels of change, they are based on only two samples taken in one area and therefore cannot be considered an adequate basis for drawing firm conclusions about the widespread declines. There is other support for the conclusion that juvenile survival has been low in Steller sea lions. In 1987 and 1988, 424 female and 376 male pups were marked on Marmot Island in the Gulf of Alaska. During the summers of 1991 to 1993, the rookery was examined for the return of marked females and only 14 were seen—far fewer than expected based on previously estimated survival curves and age-specific pregnancy rates (R. Merrick, personal communication). These results suggest either very low survival or significant movement to other rookeries. However, none of the marked females was sighted at other rookeries and only one was seen at a different haulout site (R. Merrick, personal communication). It will be important to continue monitoring the sea lions in this study to confirm the early results, which suggest low survivorship. Two studies measured population parameters of Steller sea lions in the Gulf of Alaska during 1975 to 1978 (Calkins and Pitcher, 1982) and 1985 to 1986 (Calkins and Goodwin, 1988). Results indicated late-term pregnancy rates of 60 to 67 percent, lower than for other otariid species. For example, the pregnancy rate of cape fur seals (Arctocephalus pusillus) over age 5 is 83 percent (Butterworth and Wickens, 1990) and that of 8 to 13- year-old northern fur seals varies from about 80 to 95 percent (Trites and York, 1993). Although there was a small decline in estimated pregnancy rate from the 1970s to the 1980s, the change was not statistically significant. Thus, it is possible that the pregnancy rate of Steller sea lions was depressed even in the 1970s (Calkins and Goodwin, 1988). Because it is not certain that these rates are below normal (there are no estimates from populations that have not declined), it is difficult to know whether low pregnancy rates are contributing to the population decline. Despite these 

BIOLOGY OF HIGHER TROPHIC LEVELS 144 uncertainties, a population with low birth rates is clearly more sensitive to small changes in mortality than it would be otherwise. A number of explanations have been advanced to explain the recent declines (i.e., those since about 1980) in the numbers of fur seals, sea lions and harbor seals. These are discussed in Alverson (1992), Anonymous (1993), Calkins and Goodwin (1988), Hoover (1988a, 1988b), Loughlin (1987), Loughlin and others (1984), NMFS (1992), Pascual and Adkinson (1994), and Sease (1992). Most of the proposed causes have been rejected by previous workers. The committee's assessment of the likelihood that each proposed cause has been a significant factor is given in Table 4.18. In some cases, there are insufficient data to reasonably evaluate a factor as a cause; in other cases, data are not available at the appropriate temporal and spatial scales. Although available data are not adequate to critically evaluate alternative explanations for the declines, it seems unlikely that a single factor has been responsible for the declines in all species and over all time periods and areas. More likely, several factors are responsible for the declines, the combination of which and their relative importance may have varied over time and by species. The remainder of this section discusses those causes that have been proposed, with particular attention to those that appear most influential. The committee found that, with the exception of food, the various identified potential causes are not believed to play a major role in marine mammal declines. Disease Although capable of causing population declines (e.g., Heide-Jorgensen et al., 1992), increased mortality due to disease is not thought to have been a major factor in the observed declines of pinnipeds in the eastern Bering Sea/Gulf of Alaska area (Calkins and Goodwin, 1988; NMFS, 1992; Sease, 1992). However, the importance of disease as a factor in the declines is currently difficult to evaluate because there are no estimates of trends in disease-related deaths in these species. Monitoring disease at breeding colonies or major haulout sites is possible, but would be prohibitively costly and would likely not be very productive, especially if most mortality is occurring at sea. Pollution Chemical pollutants can negatively affect pinnipeds in a number of ways (Reijnders et al., 1993). However, there is little evidence that chemical pollution has been a significant factor in the recent populations declines (Hoover, 1988a, 1988b; NMFS, 1992). One exception to this is the Exxon Valdez oil spill, which resulted in some mortality of seals in the Prince William Sound area (Frost and Lowry, 1994). 

BIOLOGY OF HIGHER TROPHIC LEVELS 145 Table 4.18 Committee's assessment of potential causes of recent declines in abundance of fur seals, sea lions, and harbor seals in the eastern Bering Sea and Gulf of Alaska Likelihood of Involvement in Declines since 1980 Cause Fur Seal Sea Lion Harbor Seal Comment Disease Low Low Low Few data, but no evidence of increased effects that could explain declines Chemical pollution Low Low Low Few data; levels low relative to known effects in other populations Entanglement Moderate Low Low Could only have been a contributing factor in the fur seal declines Harassment Low Low Low Local effects only; not important for the geographic scale over which the declines have occurred Commercial harvest Low Low Low Could not explain observed declines beyond the mid 1970s Subsistence harvest Low Low Low Not a factor in the widespread declines Incidental take Moderate Moderate Low Contributed to the declines, but not a major factor; cannot explain continued declines Predation Low Low Low Few data; could not explain the declines, but may affect recoveries Direct climate effects on Low Low Low Cannot explain the declines survival Fishery effects on food Moderate High High Could have played a major role availability in all declines Climate effects on food Moderate Moderate Moderate Could have played a role in all availability declines Competition from fish predators Moderate Moderate Moderate Could be a major factor in the declines, given observed changes in community structure that were most likely caused by commercial fishing and environmental changes 

BIOLOGY OF HIGHER TROPHIC LEVELS 146 Entanglements Fowler (1987) concluded that entanglement of juvenile fur seals in trawl net fragments could account for the decline in the Pribilof population. However, Trites (1992) examined the evidence supporting the entanglement hypothesis and concluded that while large numbers of fur seals have no doubt died in lost and discarded fishing gear, it is unlikely that entanglement has been the major cause of the decline. Steller sea lions also become entangled in packing bands and net fragments, but available data indicate that entangled adults are rarely seen, and entanglement rates of pups and juveniles appear to be even lower than those observed for adults (Loughlin et al., 1986). Based on the admittedly limited data, it is unlikely that entanglement in debris is a major factor in the decline of this species (NMFS, 1992). Entanglement of harbor seals in lost or discarded net fragments has not been observed at Tugidak Island (Pitcher, 1990), the site of the most dramatic decline in numbers, or in the Aleutian Islands (Loughlin et al., 1986). Human Disturbance and Takings Human disturbance of rookeries and haulout sites can have negative effects on pinnipeds (see review by Reijnders et al., 1993). The sites used by pinnipeds in the Bering Sea and Gulf of Alaska are generally in areas that are relatively remote or are protected from human activities. Direct human taking of marine mammals is now limited almost exclusively to subsistence hunting and to incidental kills by commercial fisheries. Based on the results of a simulation model, Trites and Larkin (1992) concluded that direct kills of sea lions in commercial harvests reduced some rookeries and may have stabilized the number of sea lions breeding in the Gulf of Alaska and Aleutian Islands. The commercial harvests, coupled with subsistence harvests and intentional and incidental kills by fisheries, would have had some depressing impact on the population up to about 1980. However, the model indicated that since 1980 over 10,000 sea lions per year were disappearing from the population, and even the highest estimates of fishery kills could not account for these missing animals (Trites and Larkin, 1992). Based on simulation modeling, Pascual and Adkinson (1994) concluded that the observed declines were unlikely to be the result of pup harvests. Merrick et al. (1987) came to the same conclusion. Population declines in northern fur seals of greater magnitude than those observed recently have occurred in the past century at the Pribilof Islands, as a result of commercial overexploitation (Kenyon et al., 1954). The recent decline in pup production at the Pribilof Islands from the mid-1950s to about 1970 can reasonably be explained by the commercial harvesting of adult females between 1956 and 1968 and a series of years of poor juvenile survival (Eberhardt, 1981; Trites and Larkin, 1989; York and Hartley, 1981). The reason for this poor juvenile survival is not known. The continued decline through the early 1980s at St. Paul Island and to the present at St. George Island cannot be explained by the commercial harvest of juvenile males that occurred until 1985 on St. Paul and until 1972 on St. George. While the data collected by fishery monitoring programs are incomplete, it is unlikely that incidental takes of fur seals have been large enough to be a significant factor in the population decline (NMFS, 1993a). 

BIOLOGY OF HIGHER TROPHIC LEVELS 147 Subsistence harvests of harbor seals in the Aleutian Islands and south-central and southeastern Alaska in the late 1960s were estimated to be roughly 5,000 annually (Hoover, 1988a). Approximately 4,000 phocid seals, including an unknown number of harbor seals, were also taken in Bristol Bay and the Yukon-Kuskokwim region (Hickok, 1978, cited Hoover, 1988). Since 1972, subsistence takes appear to be lower, and probably do not exceed 3,000 per year (Hoover, 1988a; Pitcher, 1984; Wolfe, 1993). It is unclear whether recent subsistence harvests had a local effect in recent declines in seal numbers. Bounty harvests in Alaska varied from about 6,000 to 24,000 seals annually between the 1930s and 1950s. A commercial harvest that developed during the 1960s had peak harvests of between 40,000 and 60,000 seals annually, and by 1967 harvest stabilized at 8,000 to 10,000 annually. Commercial harvesting ended in 1972 (see review in Hoover, 1988a). The influence of these harvests on population size is not known, but their effect on population trend should have ended by the late 1970s. The decline of harbor seals at Tugidak Island began in the mid-1960s and was influenced by commercial harvests, mainly of pups, between 1964 and 1972. However, the population continued to decline in the absence of commercial harvests, and after the effect of the harvests would have passed through the age structure of the population (Pitcher, 1990). The continued decline of harbor seals at Tugidak Island cannot be explained by the harvest history of this population. There are no estimates of the total number of harbor seals killed as a result of fishing operations (Sease, 1992). Recent observer and logbook data suggest that a minimum of several hundred harbor seals were killed as a result of encounters with fishing operations (Sease, 1992). Possible local or regional effects of these takes on harbor seal numbers are unknown. Predation Killer whales and sharks are probably the only significant natural predators of the pinnipeds whose populations have declined. While sharks are known to be major predators of pinnipeds in some other areas (e.g., Ainley et al., 1985; Brodie and Beck, 1983), such interactions appear to be rare in the Gulf of Alaska and Bering Sea. Predation on pinnipeds by killer whales has been documented in the Bering Sea, and there have been some recent changes in killer whale activities (Frost et al., 1992). Although there are no estimates of total predation mortality on Bering Sea/Gulf of Alaska pinnipeds, it is unlikely that increased predation could account for the declines, particularly the widespread declines in Steller sea lions (NMFS, 1992). However, predation could have some effect on the recovery of the currently reduced populations. Direct Climate Effects on Survival The possible direct effects of weather on pinniped survival are poorly known. Scheffer (1981) reported large numbers of dead northern fur seal pups on the Oregon and Washington coasts after a period of severe storms. LeBoeuf and Condit (1983) documented significant mortality in young northern elephant seals as a result of storm-driven waves. Studies on captive animals have shown that California sea lions cannot rely on physiological mechanisms alone to avoid hyperthermia at air temperatures above 22°C (Whittow et al., 1972; Whittow, 1987). A 

BIOLOGY OF HIGHER TROPHIC LEVELS 148 number of pinniped species are known to alter behavior to avoid thermal stress which could result in increased mortality, particularly in pups (e.g., Francis and Boness, 1991; Gentry, 1973; Heath, 1989; Limberger et al., 1986). However, species such as the northern fur seal and Steller sea lion can tolerate a wide range of environments from the cool, wet summers that occur in the Bering Sea to the hot, dry summers of southern California. Several approaches have been used to study the direct effects of climate on the survival of northern fur seals. Trites (1990) used a physiological model to investigate the weather conditions that pups can tolerate during the first week of life on land. The results of this work indicate that healthy, average-sized pups on the Pribilofs can tolerate any combination of wind speed, temperature, and humidity recorded since the mid-1950s. However, the model suggested that pups of low birth weight could have reduced survival during periods of cold, wet, and windy weather. Overall, these results suggest that direct effects of weather are unlikely to cause increased pup mortality in northern fur seals, or in the larger, newborn Steller sea lions and harbor seals, during their time on land. However, as Trites (1990) and others have noted, a second critical stage in juvenile survival is the transition from land to the sea. Survival of male northern fur seals from weaning to two years of age is only about 40 percent, with most deaths thought to occur in the first winter (Lander, 1979). As water conducts heat 25 times more effectively than air, thermoregulation is energetically more costly for young pinnipeds when they are at sea. York et al. (in press) used cross-correlation analysis to investigate possible relationships among juvenile (i.e., less than two years of age) northern fur seal survival and air and sea surface temperatures. Although estimates of early survival on land and at sea were significantly correlated with the environmental indices, the pattern of correlations did not provide convincing clues about the underlying mechanisms. In general, the analysis suggested that environmental conditions had a greater influence on survival at sea than on land. These results are consistent with the results of physiological modeling and observations that young northern fur seals appear to have difficulty in maintaining body temperature at low seawater temperatures (Trites, 1990). Pups lose almost 50 percent of their body mass during the first winter at sea (Scheffer, 1981). Thus, there is some reason to believe that changes in ocean temperature could affect survival of young pinnipeds. Climate events, such as El Niño, can have marked effects on pinniped populations, which are mediated through impacts on the availability of food (Trillmich and Ono, 1991). The 1982–83 El Niño event produced drastic changes in the marine environment off the west coast of North America, and detailed studies were done to document the effects on some species of pinnipeds (Trillmich and Ono, 1991). El Niño had a measurable effect on California sea lion pup production and growth rates in southern California (DeLong et al., 1991). However, the result was only a pause in the long-term pattern of population growth, and this pause was compensated for by a faster rate of increase in pup production after the El Niño than before (Boveng, 1988a). A study that compared effects of the 1973, 1983, and 1992 El Niño events on Steller sea lions at Año Nuevo Island concluded that there was some indication of limited prey availability in 1992 (Hood et al., 1993). Simulation models indicate that short-term stochastic environmental fluctuations have very likely not been responsible for the recent sea lion decline (Pascual and Adkinson, 1994). 

BIOLOGY OF HIGHER TROPHIC LEVELS 149 Life History Patterns Pinniped reproductive and foraging strategies are constrained by the need to give birth on land or ice and to obtain food from the sea (Bartholomew, 1970). Pinnipeds must also seek a solid substrate during the annual molt of their pelage, and they may haulout at other times of the year as well. This dependence on land can result in a spatial and temporal separation between seals and their food (Bartholomew, 1970). The extent of this separation is likely to vary seasonally, and to affect males and females of different ages in different ways. Thus, the effect of changes in food availability is most likely a complex function of many factors, including the age and sex of the individual and the season. Of the three pinniped species known to have declined in abundance, two are members of the family Otariidae (northern fur seal and Steller sea lion), and one is a member of the family Phocidae (harbor seal). These two groups have very different maternal reproductive strategies: otariids exhibit a "foraging cycle strategy," whereas phocids typically exhibit a "fasting strategy" (see reviews in Bonner, 1984; Costa, 1991). The foraging cycle strategy of otariids is characterized by females having moderate energy stores on arrival at the rookery that are used to support maternal and offspring requirements during a short perinatal fast (Costa et al., 1988). This is followed by regular feeding trips at sea alternating with brief visits to the rookery to nurse young over a period lasting from four months to more than a year. Thus, there is a long period of maternal care during which the foraging success of mothers has direct consequences for the growth and survival of offspring. In contrast, when the larger phocid species give birth, they have large maternal energy stores that are sufficient to support maternal maintenance and the cost of lactation over a 4- to 50-day nursing period (Bowen, 1991; Oftedal et al., 1987). This strategy reduces the reliance of females on food availability during the period of maternal care. Although the harbor seal is a phocid, recent studies have shown that females are not large enough to store sufficient reserves to support the energetic cost of lactation, and thus they need to supplement energy stores by beginning to feed after a perinatal fast of about one week (Boness et al., 1994; Bowen et al., 1992). Therefore, as for both northern fur seals and Steller sea lions, the growth and survival of harbor seal pups is likely to be affected by the foraging success of females during the lactation period. Adult male otariids are typically much larger than adult females, and as a result they have greater daily energy requirements, and perhaps larger and/or different forage areas, than females (French et al., 1989; Stewart and DeLong, 1993). Harbor seal adults of both sexes are similar in size and thus might be expected to have similar foraging ranges. Adult male otariids establish and defend territories on rookeries and do not feed for several weeks during the breeding season. The breeding biology of harbor seals is poorly known, but male seals spend much of their time in the water during the breeding season, and they therefore are not precluded from feeding. Distribution patterns may also influence the response of pinnipeds to food limitation. Northern fur seals that pup and breed in the Bering Sea undertake an annual migration that takes them out of the area, whereas both Steller sea lions and harbor seals are year-round residents of the Bering Sea and Gulf of Alaska. Thus, the population dynamics of northern fur seals will be influenced by events that occur both in the Bering Sea and elsewhere in the North Pacific. Steller sea lions and harbor seals, on the other hand, are more likely to be affected by regional conditions. 

BIOLOGY OF HIGHER TROPHIC LEVELS 150 Food Fishery Effects on Pinniped Foods The key to understanding the effects of fisheries on pinniped populations most likely lies in understanding the spatial and temporal scales that are critical to the nutrition of individual animals. Normal growth and survival of individuals depends on minimum levels of resources being available at a particular times and places, and not on mean abundance of those resources over some large area such as the eastern Bering Sea. Thus, determining that the mean abundance of food at large spatial scales, as is typical in fishery resource assessments, is likely to be at or above the requirements of a pinniped population may be not only uninformative but in fact misleading. Pinnipeds and modern offshore fishing fleets differ greatly in their abilities to determine the distribution and abundance of fishes in the ocean, and to capture them. To date, there has been inadequate attention to the importance of scales in the analysis of nutritional requirements of pinnipeds in the Bering Sea and Gulf of Alaska. After reviewing the available information on the temporal and spatial pattern of declines in Steller sea lions and harbor seals, and the pattern of fishing in areas that are thought to be important feeding locations for these species, one can hardly avoid the conclusion that the removal of fish biomass from these areas has in some way contributed to the declines, at least on localized bases. Analysis of the distribution of fishing effort in the Gulf of Alaska led NMFS to the same conclusion (Fritz, 1993b). The exact nature of these fishery effects cannot be determined from the sparse available data. However, they likely include the direct effects of reduced biomass of prey needed by pinnipeds and indirect effects on community structure that may have resulted in reduced availability of alternative prey (see Chapter 6). A recognition of the importance of considering scale with respect to food requirements of Steller sea lions is reflected in the establishment, in 1992, of fishing exclusion zones around important Steller sea lion rookeries. As stated by Fritz (1993b), "NMFS concluded that spatial and temporal concentration of trawl fishing for pollock in the 1980s could have contributed to the decline in the sea lion population." Thus, year-round exclusion zones of 10 nautical miles were placed around 37 sea lion rookeries, and zones of 20 nautical miles were established around 6 rookeries in the eastern and central Aleutians from January 1 to April 15 during the pollock roe season (Fritz, 1993). It is premature to attempt an evaluation of the effects of these exclusion zones on Steller sea lion population trends in these areas. However, it may be useful to consider the following points. First, it is unfortunate that these exclusion zones are not being designed and used in an experimental way to ensure that maximum knowledge is derived from their use. With the current approach, it will likely be impossible to determine whether changes in sea lion populations are a response to these zones or to changes in other factors. Second, recent work on the distribution of foraging (Merrick and Loughlin, 1993) suggests that these exclusion zones may be too small to effectively separate the local effects of trawlers on sea lion prey from foraging sea lions. 

BIOLOGY OF HIGHER TROPHIC LEVELS 151 Diets and Food Limitation A reasonable understanding of the composition of diets is necessary to determine how populations satisfy their energy requirements and whether or not they are limited by food availability. It is difficult to accurately describe pinniped diets for a number of reasons, however. Pinnipeds spend much of the year at sea, where it is costly or impossible to observe them. Prey size and species composition of the diets are usually derived from fish otoliths and other hard structures recovered from stomach contents or feces, but such analyses can result in a biased view of prey consumption (Dellinger and Trillmich, 1988; Harvey, 1989; Jobling, 1987; Jobling and Breiby, 1986; Murie and Lavigne, 1985). For wide-ranging species, data collected at or near coastal haulout sites may not adequately represent prey consumed offshore (Bowen et al., 1993). Diets may also differ seasonally and throughout the geographic distribution of the species. Finally, diet composition of pinnipeds may vary in response to both the absolute and the relative availability of the prey (e.g., Bailey and Ainley, 1982; Sinclair et al., 1994). In addition to these inherent limitations, dietary information for eastern Bering Sea and Gulf of Alaska pinnipeds suffers from irregular and inadequate sampling, especially in recent years (see reviews in Lowry et al., 1982, 1989). Available data on the diets of Steller sea lions, northern fur seals, and harbor seals are summarized in Tables 4.9, 4.11, and 4.13. There is some evidence to suggest that Steller sea lions diet had changed over time, with pollock becoming a more important food in mid 1970 and mid 1980 samples (Calkins and Goodwin, 1988). Calkins and Goodwin also indicate that pups consume somewhat smaller pollock than older animals, and it is likely that the proportion of small pollock in their diet increased in the 1980s (Merrick and Calkins, in press). However, sample sizes in most of these studies are too small to provide much confidence in such conclusions. Furthermore, few data are available through the 1980s to address the question of changes in diet. Considerably more is known about the diet of northern fur seals, but even here there is little recent information. Our knowledge of diets of harbor seals in the Bering Sea is scanty, and the good studies in the Gulf of Alaska are more than 20 years old. Thus, even if food is limiting, it seems clear from the above analysis that we will not find evidence for this by examining trends in the species composition of the diets of any of these species. Data suitable for such an analysis simply do not exist. Other Evidence of Food Limitation The ''Is It Food?" workshop (Anonymous, 1993) considered a number of demographic, behavioral, and physiological responses that might be taken as evidence of there being insufficient food to meet the energy requirements of declining pinniped populations in the Bering Sea and Gulf of Alaska. Following that approach, those that the committee considered might be particularly informative with respect to the food limitation hypothesis are listed in Table 4.19. Individually, these responses would be consistent with a number of alternative hypotheses and would not in themselves allow the conclusion that food limitation was responsible for the responses. However, the combinations of these responses, together with information on other potential sources of morbidity or mortality (i.e., pollutants, parasites, and disease), could 

BIOLOGY OF HIGHER TROPHIC LEVELS 152 provide more convincing evidence that food was indeed limiting. For example, reduced fecundity could be a result of food limitation, but it could also result from ingestion of high levels of polychlorinated biphenyls, chemicals that are known to cause reproductive failure (Reijnders, 1986). However, in the absence of certain levels of pollutants or other agents known to cause reproductive pathology, we are more likely to conclude that food limitation was responsible for reduced fecundity. The evidence concerning food limitation for three species of pinnipeds is discussed below. Northern Fur Seals The northern fur seal is mainly a summer resident of the Bering Sea. After the breeding season all age groups undertake migrations which take them, for the most part, to other areas of the North Pacific (see review in French et al., 1989). In general, rapid growth or fattening occurs during a one-to-three month period before the seals arrive on the Pribilof Islands in July. During the rest of the year, fur seals gradually lose body mass and condition (Trites and Bigg, 1992). Although fur seals do feed in the Bering Sea, there is no evidence to suggest that food is limited in that area. In fact, available data suggest that during the fourth-month lactation period, a time of high energy expenditure, adult female foraging trips were shorter during the 1980s, which could indicate that food was relatively more abundant, or that food was closer to the Pribilof Islands than it was earlier (Loughlin et al., 1987). Pup body mass at two months of age has also increased over time, suggesting an increase in food availability for lactating females (Fowler, 1990). The size of juveniles returning to the Pribilof Islands has also increased in recent years (Baker and Fowler, 1992). All of these observations have been interpreted as density-dependent responses to reduced competition for food (Fowler, 1990). Furthermore, since 1984 pup production on St. Paul, where most pups at the Pribilof Islands are born, has been relatively stable (York, 1990), suggesting an improvement in survival and/or reproductive rates. Recent studies indicate that pups generally leave the Bering Sea within two weeks of weaning (Ragan et al., 1993), such that they are reliant on food resources in the eastern Bering Sea for only a brief period. It has been suggested that low availability of food in the Aleutians could compromise pups as they leave the Bering Sea (Trites, 1992). At present, there are no data to support this speculation, which stems from the temporal correspondence between the rapid development of commercial fisheries in the early 1970s and the "unexplained" continued decline of the fur seal population. It is also possible that large-scale changes in ocean climate have reduced winter food availability in areas of the North Pacific outside of the eastern Bering Sea, through effects on either prey population abundance or distribution. Large-scale changes in the environment are known to have occurred in the North Pacific (see Chapters 3 and 4). However, it is not possible to directly relate these changes to the survival of fur seal juveniles. 

BIOLOGY OF HIGHER TROPHIC LEVELS 153 Table 4.19 Demographic, behavioral, and physiological responses that could indicate food limitation in pinnipeds Factor Expected to Change Observed Change Northern Fur Seal Steller Sea Lion Harbor Seal Lower birth mass Unknown No change Unknown Reduced growth rate Increased Reduced Unknown Reduced body condition Increased Reduced Unknown Reduced milk production/intake Unknown Unknown Unknown Increased foraging trip duration Decreased No change Unknown Reduced weaning mass Increased No change Unknown Reduced juvenile survival Reduced Inferred Unknown Increased age at first birth Unknown Maybe Unknown Decreased birth rate Unknown Maybe Unknown Reduced adult survival Inferred Inferred Unknown Source: Committee on the Bering Sea Ecosystem. Steller Sea Lions Two lines of evidence have been used to support the hypothesis that food limitation may be responsible for the population decline of Steller sea lions. Calkins and Goodwin (1988) compared size-at-age data for sea lions in the Kodiak area in 1985–86 with similar data for animals collected during 1975–78 (Calkins and Pitcher, 1982). They found that sea lions 1 to 10 years old were shorter and leaner and weighed less in the 1980s than those examined during the 1970s. With the declining trend in population size over this period, a density- dependent increase in size at age should have occurred if the overall amount of food available for sea lions had remained constant. The decreased growth rates suggest that food availability must have declined more than population size. Although this conclusion appears to be warranted, it is important to remember that it is based on limited data from only one area where sea lions have declined. Similar comparisons have not been made in southeast Alaska where the sea lion population has increased. The second line of evidence indicating nutritional stress was a reduction in hemoglobin levels in seal lions examined during the 1980s compared to those sampled in the 1970s (Calkins and Goodwin, 1988). Hemoglobin level is a useful indicator of anemia, dehydration, or iron deficiency (Bossart and Dierauf, 1990). However, the mean levels measured in Steller sea lions in both periods are well within normal ranges reported for several other otariid species (Bossart and Dierauf, 1990) and for Steller sea lion pups two to three weeks of age (Castellini et al., 

BIOLOGY OF HIGHER TROPHIC LEVELS 154 1993). Although the normal range of erythrocyte indices has not been established for Steller sea lions, the suggestion that sea lions in the 1980s sample were anemic is equivocal. The hypothesis that reduced survival of juveniles may be the cause of the population decline (York, 1994) is attractive because recent studies have shown that weaned pups have limited foraging abilities compared to older sea lions (Merrick and Loughlin, 1993). Using satellite-linked, time-depth recorders, Merrick and Loughlin (1993) studied the foraging ranges and diving behavior of 19 adult female sea lions and 5 pups. They found that during the summer adult females with pups generally foraged within 20 km of land, made brief trips of less than two day's duration, and dived to depths of 830 m. In winter, some females traveled over 300 km offshore for up to several months and often dived to >250 m. Pups, on the other hand, were able to cover more than 300 km in a trip but their dives were generally brief (less than 1 minute) and shallow (less than 20 m). These preliminary results suggest that pups may rely heavily on prey near the surface, and that small changes in prey abundance in near-surface waters may have large effects on pup foraging success and thus on pup survival. There is also evidence that, like other pinnipeds, sea lion pups consume smaller prey than those taken by older sea lions (Merrick and Calkins, in press; Lowry et al., 1989). This may further constrain the array of prey available to pups compared to older animals. Based on studies on other pinniped species (e.g., Costa et al., 1989); Trillmich and Ono, 1991), one would expect changes in the availability of food to be reflected in the foraging behavior of lactating female sea lions and the growth and behavior of their suckling offspring. However, when Davis et al. (1993); Merrick et al. (1995) compared data for a declining population at Chirikof Island to data for a stable population at Lowrie Island they found no significant difference in female foraging trip duration, pup birth mass, or pup growth rates between the two areas. This suggests that mothers are not food-limited during the early part of lactation. Given the long period of maternal care in this species, it is possible that the effect of food limitation on lactating females and pups may become evident only later in lactation. Thus, further study is needed to determine both interannual variation and how these patterns may change during the entire lactation period. As noted earlier, pregnancy rates in Steller sea lions are lower than for other otariids for which data are available. It is not known whether low food availability is a contributing factor to these relatively low rates. It may be significant, however, that adult Steller sea lions consume more fish of the size range removed by commercial fisheries than do other Bering Sea pinnipeds (Lowry and Frost, 1985; Lowry et al., 1989). Harbor Seals There are no data that can be used to examine the hypothesis that food limitation has caused or contributed to the decline in the number of harbor seals in the Bering Sea or Gulf of Alaska (Table 4.19). A reasonably comprehensive study was conducted in the late 1970s to describe the biology of this species (Pitcher and Calkins, 1979). However, virtually no biological research was conducted on the biology of Alaskan harbor seals between then and the time of the Exxon Valdez oil spill in 1989. Recent studies initiated in response to the oil spill 

BIOLOGY OF HIGHER TROPHIC LEVELS 155 and the general population decline may provide some insight into factors affecting harbor seals in these areas.