FOOTNOTES:

[52] Present address: U.S. Fish and Wildlife Service, Office of Biological Services—Coastal Ecosystems. 1011 E. Tudor Road, Anchorage, Alaska 99503.

[53] This figure is based on data through 1971. Since then, the number of catcher-boats has decreased to 332 in 1974 (F. M. Fukuhara, personal communication).

[Interactions Among Marine Birds and Commercial Fish in the Eastern Bering Sea]

by

Richard R. Straty and Richard E. Haight

National Marine Fisheries Service
Auke Bay Fisheries Laboratory
Auke Bay, Alaska 99821

Abstract

The high primary and secondary productivity of the eastern Bering Sea makes it one of the greatest producers of commercial fish and largest congregating areas of marine birds in the world. The fish and birds are so interrelated that fluctuations in the abundance of one may well be responsible for changes in the abundance of the other. The seasonal and annual variation in the impact of birds on fish is a function of the life history, food habits, growth rate, and final size of the fish species of concern and of the distribution, abundance, and feeding habits of bird populations—plus the effects of the environment on these factors. Stages in the life history of some of the important commercial fish and shellfish of the Bering Sea directly or indirectly influenced by marine birds are identified.

The eastern Bering Sea is one of the world's richest fish-producing areas and is also one of the world's major congregating areas for marine birds. The large extent of the continental shelf and the climatic and oceanographic characteristics of the eastern Bering Sea combine to make this region extremely productive biologically. The distribution and abundance of plankton, benthos, and fish determine the distribution, time, and character of the migration of marine birds in the eastern Bering Sea (Shuntov 1961). Several studies have illustrated the close relation between marine birds and the biological properties of surface waters (Tuck 1960; Bourne 1963; Solomensen 1965). Spatial and temporal variations in the abundance of the fish families Clupeidae (herring), Gadidae (codfish), Osmeridae (capelin), and Ammodytidae (sand lance) are thought to be major determinants of the breeding seasons, breeding places, and movements of boreal seabirds (Ashmole 1971). The timing of breeding among larids and alcids is related to the seasonal changes in the surface waters inhabited by Ammodytidae and Clupeidae in the North Sea (Pearson 1968).

The eastern Bering Sea contains members of these and other fish families that are extensively exploited by man; the fish are also important as forage for other species of commercial fish, marine mammals, and marine birds. During some part of their life cycles, all fish species feed on plankton, nekton, benthos, or other fishes.

The incidental use or dependence of marine birds on commercial fish and the items on which the fish feed account for the major interaction between man and these two groups of animals.

In this paper, we consider how marine birds and fish interact. Although some of what we present is only speculative, we identify certain areas that have received little or no scientific study, areas in which further research is needed for a better understanding of the role of commercial fish in the ecology and dynamics of marine birds in the eastern Bering Sea.

Commercial Fish Resources of the Eastern Bering Sea

Most of the fishing in the eastern Bering Sea is done by Japan and the Soviet Union. Japan resumed fishing in the Bering Sea in 1953 (7 years after World War II), the Soviet Union started fishing in the region in 1959, and since the early 1960's both nations have accelerated their exploitation of Bering Sea fish stocks (Chitwood 1969).

Species of major concern to Japan and the Soviet Union include fish—walleye pollock (Theragra chalcogramma), yellowfin sole (Limanda aspera), Pacific cod (Gadus macrocephalus), Pacific ocean perch (Sebastes alutus), Pacific herring (Clupea harengus pallasi), and sablefish (Anoplopoma fimbria)—and snow crabs (Chionoecetes spp.). The distribution of the principal species being harvested in Bristol Bay and the eastern Bering Sea are shown in Figs. 1, 2, and 3. The weight of each of the major species in the total catches made by foreign and domestic fishermen in 1973 is shown in Table 1. In 1972, the catch of commercial finfish in the eastern Bering Sea alone amounted to 5% of the total world catch of marine fishes (H. Larkins, personal communication).

Most species of commercial fish in the Bering Sea are in a state of decline or in a depressed condition from overexploitation (Table 1). This is indicated by a reduction in the catch per unit of effort and in the mean size of fish in the commercial catch (H. Larkins, personal communication). The notable exception is the king crab (Paralithodes sp.), which has increased in abundance in recent years as a result of reduced foreign fishing.

Table 1. Foreign and domestic catch of fish and shellfish in the eastern Bering Sea, including Bristol Bay, 1973.
SpeciesCatch (metric tons)
Fish
Pollock1,500,000
Flatfish125,000
Pacific cod45,000
Herring35,033
Salmon11,785
Sablefish7,000
Pacific halibut222
Other40,000
Shellfish
King crabs26,798
Snow crabs17,694
ShrimpMinor

Fig. 1. Areas of major concentrations of ground fish (Pacific pollock, halibut, yellowfin sole, rock sole, flathead sole, Pacific ocean perch, and Pacific cod) in Bristol Bay and the Bering Sea.

Fig. 2. Areas of major winter and spring concentrations of Pacific herring in Bristol Bay and the Bering Sea.

Fig. 3. Areas of major concentrations of king and snow crab in Bristol Bay and the Bering Sea.

Routes of Interaction Between Marine Birds and Commercial Fish

The obvious ways in which marine birds and fish of commercial importance interact in the eastern Bering Sea are illustrated by the simplified food web diagram in Fig. 4. The major animal groups and species included in two of the categories in this figure—secondary producers (invertebrate forage) and intermediate carnivores (commercial and forage marine fish and shellfish)—are as follows:

Fig. 4. Food web in the eastern Bering Sea, showing routes of interaction between marine birds and the various life history stages of commercial fish and shellfish.

In our discussion, we mainly consider predation by birds on commercial fish and competition between birds and commercial fish for food. The extent of these interactions determines the potential for birds and fish to influence each other's abundance. The extent of the interactions also determines the impact of man's commercial harvest of fish on the abundance of birds or of the bird's harvest on the abundance of fish.

The extent of the interaction between marine birds and commercial fish depends on the abundance, distribution, feeding habits, and life history of the fish species of concern. We have limited our discussion to examples of the major commercial pelagic and demersal fish and shellfish of the eastern Bering Sea. We also use as examples those species of marine birds whose abundance in the eastern Bering Sea and feeding habits give them the greatest potential for influence on, or being influenced by, fish abundance.

Abundance and Feeding Habits of Marine Birds in the Eastern Bering Sea

Information on the general abundance and distribution of the most important marine birds in the eastern Bering Sea in the summer and winter is scattered among many published and unpublished reports: Shuntov (1961, 1966), Sanger (1972), Bartonek and Gibson (1972), and Ogi and Tsujita (1973); and surveys by D. T. Montgomery and W. E. Oien ("Bristol Bay waterbird survey, 1972," unpublished report of the U.S. Bureau of Sport Fisheries and Wildlife, Alaska area) and by J. G. King and D. E. McKnight (1969, "A waterbird survey in Bristol Bay and proposals for future studies," unpublished report of the U.S. Bureau of Sport Fisheries and Wildlife and the Alaska Department of Fish and Game, Juneau, Alaska).

In summer, the most abundant birds appear to be the procellariids, mainly the slender-billed shearwater (Puffinus tenuirostris) and Pacific fulmar (Fulmarus glacialis); the alcids, mainly the common murre (Uria aalge), thick-billed murre (U. lomvia), tufted puffin (Lunda cirrhata), horned puffin (Fratercula corniculata), and the ancient murrelet (Synthliboramphus antiquus); and the larids, mainly the glaucous-winged gull (Larus glaucescens) and the black-legged kittiwake (Rissa tridactyla).

In winter, the alcids and larids appear to be the most abundant groups, the procellariids having been reduced by the departure of the slender-billed shearwaters for breeding grounds in the southern hemisphere. The selection of the types of food to be consumed by these marine birds is a function of their morphological and physiological adaptations and of the resultant feeding behavior. Ashmole (1971) classified the feeding behavior of various genera of marine birds and the relative importance of the kinds of food eaten by each group; this information for some of the Bering Sea bird species occurring in the genera listed by Ashmole (1971) is summarized in Fig. 5.

Fish and invertebrates are evidently of moderate to major importance in the diet of these marine birds (Fig. 5). The extent to which a given fish species is fed upon by or is in competition with marine birds for food is determined by the life history of the fish. Most pelagic and some demersal fish and shellfish are more subject to predation by pursuit diving birds than by birds restricted to the near-surface waters. Invertebrates appear to be equal to or more important than fish in the diets of birds feeding in near-surface waters (Fig. 5).

Predation by Marine Birds

The literature contains numerous accounts of marine birds feeding on marine fish and shellfish of commercial importance. Some studies quantify the impact of some bird species on certain species of commercial fish (Outram 1958; Shaefer 1970; Wiens and Scott 1976) and shellfish (Glude 1967). Other studies have shown that in some regions the value of guano produced by birds may exceed the value of the commercial fish they consume (Jarvis 1970). Some fish of worldwide commercial importance that are important in the diets of marine birds are listed in Table 2.

FishShearwaters Murres Puffins Fulmars Gulls
Anchovy X————
Sardines X————
Herring X X X X X
Sprat X————
Pilchard X————
Capelin— X X— X
Salmon— X———
Mackerel— X———
Pollock— X— X—
Haddock— X———
Cod— X———

The significance of bird predation on pelagic or demersal fish and shellfish (Fig. 5) depends on the feeding behavior of the birds and on the life history of the fish (e.g., distribution, abundance, growth, and adult size). Pursuit diving birds, such as murres and puffins, can consume fish at greater depths than can birds that feed near the surface, such as shearwaters, kittiwakes, fulmars, and gulls.

Fig. 5. Feeding behavior and relative importance of food of some groups of marine birds that occur in the eastern Bering Sea.

Aspects of the Life Histories of Fish Related to Predation by Marine Birds

Fish that are pelagic during part of their lives, such as salmon and herring, and forage fish like smelt, capelin, and sand lance, are vulnerable to greater predation by a wider variety of marine birds than are bottom-dwelling demersal fish, such as pollock, cod, sole, ocean perch, and halibut, as well as king and snow crabs. Some species that live on the bottom as adults have pelagic stages during which they are vulnerable to predation by marine birds. Juveniles of some demersal species (pollock, cod, halibut, some species of sole, and king crabs) are sometimes found in shallow water where they might be subject to predation by birds.

Demersal Fish and Shellfish

The early life histories of the commercially important demersal fish of the eastern Bering Sea are quite different (Table 3). For example, the eggs and larvae of Pacific halibut (Hippoglossus stenolepis) generally occur at depths greater than 100 m (Hart 1973), whereas those of pollock and yellowfin sole are found at or near the surface (Musienko 1963, 1970). The eggs of Pacific cod are demersal, but the larvae are oceanic (pelagic) and occur from 25-150 m (Mukhacheva and Zviagina 1960).

In their juvenile stages, many demersal fish frequent the near-surface waters (Table 3), where they become vulnerable to predation by piscivorous marine birds. Juvenile pollock, for example, form into small schools that usually move about close to the bottom but sometimes move into areas as shallow as 3 m. Juvenile Pacific cod prefer the warmer water close to shore and may be found within 10 m of the surface (Moiseev 1953). The young of many species of flatfish, such as yellowfin sole, rock sole (Lepidopsetta bilineata), and flathead sole (Hippoglosoides elassodon), remain for a time in shallow warm water after assuming a demersal existence. Yellowfin sole 2-2.5 cm in total length may be found in abundance in areas as shallow as 5 m (Fadeev 1965; Moiseev 1953).

Table 3. Informal listing of life history information on selected species of commercial and forage fish and shellfish to show vulnerability to predation by marine birds. (? indicates no information available.)
FecunditySpawning season
Length of female (cm)[54]Mean no. of eggsTotal periodPeak periodLife stageTotal length
(cm)[56]		Depth from surface
(m)		Seasonal period of pelagic lifeDuration of life stages
(days)		Source of data
Walleye pollock (Theragra chalcogramma Pallas)
31-3595,700Feb.- JuneApril-MayEgg0.1-0.20-10Feb.-June12 at 6-7°CYusa 1954; Tanino et al. 1959; Kobayashi 1963; Musienko 1963, 1970; Serobaba 1968; Hart 1973[55]
20.5 at 3.4°C[57]
Larval0.4-0.910-25March-?> 25 at 6-7°C
46-50324,400——Larval0.9-?25-??-Sept.?
————Juvenile2.2-4.10-?[58]Summer—
————Juvenile6.0-30.04-37Summer—
————Adult30.0-70.00-386——
Pacific cod (Gadus macrocephalus Tilesius)Egg0.1-0.11100-250Demersal8-9 at 11°CMoiseev 1953; Mukhacheva and Zviagina 1960; Musienko 1970; Hart 1973[55]
601,200,000Jan.-March?17 at 5°C
28 at 2°C
Larval0.5-3.225-150Feb.-Aug.?
783,300,000——Juvenile?10-?Summer—
————Adult40.0-99.00-900——
Pacific herring (Clupea harengus pallasi Valenciennes)Egg0.1-0.20-12Demersal10-20[57]Stevenson 1962; Musienko 1970; Rumyantsev and Darda 1970; Reid 1972; Hart 1973[55]
20.5-22.026,600May-JuneVariesLarval0.90.5-8May-June42-56
28.0-31.077,800——Larval1.30.5-8June-July
————Larval2.51-6July-Aug.
————Juvenile2.5-20.50-?March-Nov.—
————Adult20.5-31.00-140March-Nov.—
Capelin (Mallotus villosus (Muller))Egg0.1<20Demersal14-?Clemens and Wilby 1961; Musienko 1970; Hart 1973
?3,000June-July?Larval0.5-??June-??
?6,000——Juvenile??March-Nov.(est.)—
10.36,670——
?60,000——Adult?0-?March-Nov.—
Pacific sand lance (Ammodytes hexapterus Pallas)
—?June- Aug.[59]Egg??Demersal?Musienko 1963, 1970; Kashkina 1970; Hart 1973
————Larval0.7-3.40-?June-Sept.?
————Juvenile3.6-9.60-??—
————Adult260-??—
Pacific ocean perch (Sebastes alutus (Gilbert))
2610,000March-May?Egg[61]————Paraketsov 1963; Lisovenko 1965; Lyubimova 1965; Kashkina 1970[60]
44180,000——Larval[62]0.6-?[62]March-Aug.?
————Juvenile6.237-128——
————Juvenile10.437-154——
————Juvenile14.7-21.337-230——
————Adult21.3-51.037-420——
Pacific halibut (Hippoglossus stenolepis Schmidt)
75101,723Oct.-March?Egg0.3-0.440-935Oct.-March48 at ?Novikov 1964; Hart 1973
1352,800,837——Larval0.8-1.5>200Nov.-May70-98
————Larval1.5-2.9<100May-Sept.
————Juvenile3.4-4.27-43——
————Juvenile19-257-45——
Yellowfin sole (Limanda aspera (Pallas))
26.1-28.01,295,000June-Aug.JulyEgg0.07-0.09>0June-Aug.9.4 at 13.1°C[57]Moiseev 1953; Pertseva-Ostraumova 1954; Musienko 1963; Fadeev 1965; Kashkina 1965a, 1965b[55]
40.1-42.03,319,500——Larval0.2-1.2>0July-Oct.?
————Juvenile 2.1-2.55-15——
King crabs (Paralithodes camtschatica (Tilesius))
9.455,408April-June?Egg—100-200[63]—?Kurata 1960, 1964; Korolev 1964; Rodin 1970
17.1444,651——Zoeal0.55-0.65?April-July33 at 7-10°C
————Zoeal23 at 12.3-12.5°C
————Glaucothoeal 0.38x0.18?May-??
————Juvenile?1-?—?
Snow crabs (Chionoecetes bairdi Rathbun)
???[65]?Egg—100[63]—?Haynes 1973[55] Jewett and Haight[64]
————Prezoeal0.22-0.28?May-?1-2 at 2.5°C
————1st zoeal0.50-0.56?Summer?
————2d zoeal?0-10Summer?
————Megalopal0.30-0.35x?Summer—
0.18-0.21
————Juvenile0.44-0.48x?——
0.32-0.35
Snow crabs (Chionoecetesopilio (O. Fabricius))Egg?93[60]—?Ito 1968; Kon 1970; Haynes 1973; Motoh 1973; Jewett and Haight[64]
???[65]?Prezoeal—?May-?63-66 at 11-13°C
————1st zoeal 0.48-0.54?Summer
————2d zoeal0.62-0.71?Summer
————Megalopal 0.29-0.33?Summer
————0.19
————Juvenile4.4-4.8x?——
————3.2-3.5

The commercially important king and snow crabs of the eastern Bering Sea also have larval stages that are pelagic (Table 3). Zoeae and megalopa of snow crabs are found near the surface where they are vulnerable to plankton-feeding marine birds. The eggs of king crabs are attached to the abdomen of the female, but after hatching, the larvae become pelagic and occur near the surface. They are planktonic through five larval stages before settling to the bottom to take up demersal residence (Kurata 1960, 1964). These larvae attain a length of 5.5-6.5 mm and spend 33 days or more in the plankton (Kurata 1960). Even after the young king crabs have settled to the bottom, they may still frequent water shallow enough to make them vulnerable to predation by some marine birds. Juvenile king crabs 1 and 2 years of age appear to prefer shallower water than do older crabs. In southeastern Alaska, during the spring, small juvenile crabs have been observed in pods at depths as little as 1 m below the low tide level.

The available life stages of king and snow crabs and commercially important demersal fish (Table 3) represent an enormous food supply for other fishes and marine birds. Predation by marine birds on pelagic eggs and on the larval and juvenile stages of demersal fish is not well documented, probably because the rapid digestion rate of birds makes species identification of these stages difficult. Investigators must often depend on the presence of the hard parts of fish (such as scales and otoliths) in the stomachs of birds to identify the species eaten. Because these hard parts have not yet formed in the larvae and most juveniles, predation by marine birds on older fish is more apparent on examination of stomach contents. Full understanding of predation by marine birds on demersal fish and shellfish requires additional data on when and where the egg, larval, and juvenile stages are present.

Pelagic Fish

Many fish, such as herring, capelin, smelt, and salmon, are pelagic for part of their lives, particularly during the spring and summer feeding periods. The extent of predation by marine birds on these species depends primarily on the location of their spawning grounds, their growth rates, and the size of the adults. The spawning location determines the extent of predation on eggs, whereas growth rate and adult size determine during how much of its lifetime a given fish species is vulnerable to the wide variety of marine birds.

Herring spawn in intertidal and subtidal zones and spend most of their post-larval lives in bays or estuaries near the coast. They deposit their adhesive eggs primarily on vegetation, and the eggs are particularly vulnerable to predation by a wide variety of marine and terrestrial birds. Outram (1958) estimated that gulls alone accounted for 39% of the egg loss on the spawning grounds at Vancouver Island, British Columbia. When herring larvae hatch, they are between 0.7 and 0.8 cm long; when they metamorphose about 6-8 weeks later, they are between 2.6 and 3.5 cm long. Thereafter, juvenile herring grow rapidly and reach a length of about 7-10 cm before winter. Although herring as old as 13 years and up to 38 cm long have been reported in Alaska, they seldom exceed 30 cm and 11 years of age (Rounsefell 1929). During spring and summer, herring are commonly within 10 m of the surface, but in winter, they are in water 100-140 m deep. Although herring are particularly vulnerable to predation in spring and summer, they are available to marine birds during most of their life.

The life history of capelin is somewhat different than that of herring—they live in the open sea near the surface and throughout the water column most of their lives. Sometime in June or early July, they migrate in large schools toward shore to spawn (Musienko 1970). In British Columbia, capelin bury their eggs in coarse sand and gravel in the intertidal and subtidal zones. The larvae are 0.5-0.7 cm long at hatching and are carried by currents to the open sea where they develop in the plankton. Capelin attain an age of 5 years and a maximum length of about 22 cm; their small size makes them vulnerable to predation by marine birds most of their lives, and they are an important pelagic food fish for other commercial fish in the Bering Sea.

The sand lance reaches a maximum size of 20-26 cm and is vulnerable to bird predation during most of its life. Little information is available on the maximum age attained by this species in the Bering Sea, but because of its size, it is an important forage fish for many commercial fish species.

The five species of Pacific salmon of the eastern Bering Sea spawn in fresh water, unlike herring, capelin, and sand lance. Their eggs are not vulnerable to extensive predation by marine birds; gulls take mainly salmon eggs which have been dislodged from the gravel and are drifting or being rolled along the stream bottom by the current (Moyle 1966). After a few months to several years in fresh water, the juvenile salmon (5-14 cm long) enter the Bering Sea during late spring or early summer and migrate through these waters to feeding grounds, primarily in the north Pacific Ocean. At maturity, the survivors return to their home streams and rivers to spawn. It is during the seaward migratory phase of their life cycle that salmon are most vulnerable to predation by marine birds.

The sockeye salmon (Oncorhynchus nerka) is the most abundant and valuable species harvested by American fishermen in the waters adjacent to the Bering Sea and, as a result, the one that has been most extensively studied during early marine life. Juvenile sockeye salmon are between 8 and 14 cm long when they enter the Bering Sea between late May and early July. They are most abundant in the upper 1 m of water at night and the upper 2 m during the day (Straty 1974)—well within the regime that can be exploited by many species of marine birds.

The numbers of juvenile sockeye salmon migrating seaward from the Bristol Bay region of the Bering Sea in a single year has ranged between 46.3 and 370.4 million (H. Jaenicke, personal communication). This is equivalent to between 409 and 3,267 metric tons (on the basis of the mean weight of the juveniles when they enter the Bering Sea). These large numbers of juvenile sockeye salmon, plus juvenile chinook salmon (O. tshawytscha), coho salmon (O. kisutch), chum salmon (O. keta), and pink salmon (O. gorbuscha) from all other rivers entering the Bering Sea, represent a considerable input of energy from fresh water in the form of prime forage fish for other fishes, marine birds, and mammals. Young salmon enter the Bering Sea each year over a period of only 6 to 8 weeks and may follow rather discrete coastal migration routes through the Bering Sea (Fig. 6), with the result that predators have access to an abundant but transient food supply.

Fig. 6. Distribution of juvenile sockeye salmon in Bristol Bay and the eastern Bering Sea (adapted from Straty 1974).

The only published account of predation by marine birds on juvenile salmon in the Bering Sea is that of Ogi and Tsujita (1973). They found juvenile sockeye salmon in the stomachs of murres captured in gill nets in the eastern Bering Sea. The predation did not appear extensive, but most of the birds were captured outside or on the fringes of the main seaward migration route of the salmon. The foods of marine birds should be studied in conjunction with studies of the migrations of juvenile salmon.

Influence of Growth Rate and Adult Size of Fish on the Extent of Predation

Incubation time for fish eggs, the length of the pelagic larval period (Table 3), and the growth rate of juvenile fish are species-specific and temperature-dependent. The extent to which a fish species is subjected to predation by marine birds is directly related to the rate at which development and growth occur. For example, the less time it takes the pelagic eggs of demersal fish and shellfish to hatch and complete pelagic larval life, the less is the time they will be preyed on by marine birds. For fish species that are pelagic during their entire life, the rate of growth will determine how long they remain small enough for birds to eat. Some of the smaller pelagic fish, such as herring, capelin, and smelt, are vulnerable to bird predation most of their lives; larger pelagic species like salmon may be preyed on for only a very short time. The maximum size fish that can be eaten by marine birds is, therefore, important in evaluating predation on a given species of fish.

The literature on the food habits of marine birds contains little on the sizes of fish consumed. Tuck (1960) stated that murres probably will take fish up to 18 cm long. Ogi and Tsujita (1973) estimated the lengths of Pacific pollock in the stomachs of murres taken in the eastern Bering Sea at 24 cm.

Herring in the eastern Bering Sea reach an age of 11 years and grow to about 33 cm. Herring could, therefore, be taken during most of their lives by murres but during only the first few years by smaller birds such as fulmars and shearwaters. Capelin and some species of smelt would be vulnerable to birds during all their lives. Although the size of adult Pacific salmon varies with the species, they are all so large that they are not preyed upon by marine birds. Once in the ocean, juvenile salmon grow at such a rapid rate that they are probably not very vulnerable to marine birds after their first 4 to 6 months at sea. Limited studies on the growth of juvenile sockeye salmon in the eastern Bering Sea (Straty 1974) indicate they may double their size in their first 8 weeks at sea. A sockeye salmon that entered the Bering Sea at 12 cm in mid-June would be 24 cm long in August—the maximum size that a murre could eat; the fish could be eaten by smaller marine birds for much less time. Pink and chum salmon enter the sea at a smaller size than sockeye salmon and would be vulnerable to predation both by a greater variety of marine birds and for a longer period of time.

Competition Between Commercial Fish and Marine Birds

We do not know the importance of competition between marine birds and commercial fish in the eastern Bering Sea. Only a few investigators have even alluded to competition between marine birds and fish for food. Ogi and Tsujita (1973) mentioned that competition seemed to exist between murres and juvenile sockeye salmon for euphausiids in the eastern Bering Sea. We have listed some of the types of forage fish and invertebrates eaten by commercial fish (Table 4) and marine birds (Table 5) in the eastern Bering Sea; comparison of these two tables clearly indicates that competition could occur.

The principal factors determining the extent of competition between marine birds and fish are the numbers of birds and fish, the length of time that various life history stages of the fish are in association with the birds, and the abundance of the preferred foods at these times. The impact of competition depends on the adaptability of the birds and fish to alternative types of food.

The types and sizes of food eaten by fish vary with the life history stage—especially with size at each stage. For instance, very young herring eat the eggs and nauplii of copepods or small copepodite stages and barnacles. As herring grow, their diet includes small fish and larger zooplankton, such as mature copepods, amphipods, euphausiids, and pteropods. Pacific cod shorter than 9 cm feed on small crustaceans (Moiseev 1953), whereas larger cod eat young crabs, shrimp, and fish. Small juvenile sockeye salmon feed mainly on larval stages of euphausiids (Straty 1974), but larger juveniles also eat the more adult forms, which eventually make up a significant part of their diet (Nishiyama 1974).

The change in the diet of fishes with growth results in competition with a changing variety of marine birds. For example, deep-diving birds may replace surface feeders as the major bird competitors of the Pacific cod and pollock as these fish increase in size and seek deeper waters. The diet of cod changes from small crustaceans in shallow water to progressively larger food that eventually includes herring, sand lance, shrimp, and crabs. The change to herring and sand lance, and quite possibly small crabs, places the adult cod in competition with both the surface feeders and pursuit diving birds, but adult cod do not compete with birds for zooplankton.

Table 4. Food items eaten by the adult stage of seven commercially important species of fish in the eastern Bering Sea.
Food itemHerringSalmonWalleye pollockPacific codPacific ocean perchYellowfin solePacific halibut
Invertebrates
PteropodsXX——X——
Squid—X—XX—X
PolychaetesXXXX—XX
CopepodsXXX————
AmphipodsXXXXXX—
EuphausiidsXXX—XX—
DecapodsXXXXXXX
Fish
CapelinXXXX—X—
Sand lance—XXX——X
Table 5. Forage fish and invertebrate foods eaten by seven species of marine birds in the eastern Bering Sea.
Food itemShearwatersMurresPuffinsMurreletsFulmarsKittiwakesGulls
Forage fish
Sand lanceXXX——XX
Capelin——X————
Invertebrates
Copepods—————X—
EuphausiidsXX———X—
AmphipodsXX———X—
DecapodsXX———X—
Pteropods—X—————
Chaetognaths———————
Polychaetes—XX——X—
SquidXX——X——

As pollock increase in size, they continue to feed mainly on zooplankton, but they change from copepods near the surface to euphausiids at mid-depths and near the bottom. Euphausiids are large and abundant zooplankters which, for the most part, are available only to deep-diving birds. Adult pollock also consume herring, sand lance, capelin, and other small fish.

Both marine birds and fish are capable of exploiting a wide variety of food, and often their stomach contents reflect the relative abundance of food items in the area. Ogi and Tsujita (1973) illustrated the differences in the food taken by murres captured at different locations in the eastern Bering Sea. Carlson (1977) and Ogi and Tsujita (1973) reported on differences in the diet of juvenile sockeye salmon captured at various locations in Bristol Bay and the eastern Bering Sea. The diets of many species of birds and fish, however, seem to be largely determined by their physiological and morphological adaptations and resultant feeding behavior. For instance, adult sockeye and pink salmon have well-developed gill rakers and feed largely on zooplankton, whereas chinook and coho salmon have poorly developed gill rakers and feed almost entirely on fish. In the eastern Bering Sea, murres appear to prefer the Pacific sand lance, whereas the slender-billed shearwater consumes mainly euphausiids (Ogi and Tsujita 1973). Thus, murres may be greater competitors with piscivorous fish than are shearwaters. Shearwaters are probably more important as competitors with zooplankton-eating fish that inhabit shallow water in juvenile stages and with pelagic fish species (such as pollock, herring, salmon, and capelin) that are heavily dependent on euphausiids.

Some species of marine birds may interact with fish as predators and competitors. As an example, pursuit diving birds, such as murres and puffins, may be important predators on juvenile salmon in the eastern Bering Sea, but these same birds may compete for food with adult salmon. Surface-feeding birds, such as fulmars, shearwaters, kittiwakes, and gulls, may be important as both predators and competitors with herring and capelin and some demersal fish.

Dependency of Marine Birds on Commercial Fish

The interactions of commercial fish and marine birds of the Bering Sea can be determined only if we know their distribution, abundance, and food habits, especially while they are associated with one another. Information is particularly lacking for all life history stages of commercial fish species and the seasonal movements of birds. We have some knowledge of the distribution and abundance of the various life history stages and the food habits of commercial fish in the Bering Sea. Little is known of the abundance, seasonal movements, and food habits of marine birds in this region, however, probably because marine birds have had little direct commercial value in the northern hemisphere. Food studies on marine birds are particularly difficult because their rapid digestion soon destroys the identity of the food.

We can make a reasonable guess as to some bird-fish associations for two regions of the Bering Sea where we have information on the distribution of marine birds and the various life history stages of commercial fish. For example, piscivorous birds, such as murres, puffins, black-legged kittiwakes, and slender-billed shearwaters, are extremely abundant in the summer along the seaward migration route of juvenile sockeye salmon (Fig. 7); the juvenile salmon, kittiwakes, and shearwaters all feed on plankton. Shuntov (1961) showed that kittiwakes are most abundant along the edge of the continental shelf in the Bering Sea in the summertime. This distribution coincides with the distribution of the eggs and larvae of pollock, certain flatfish, rockfish, sablefish, and several other species. These birds both exploit the fish directly (predation) and compete with them for plankton. Not enough information is available on the food habits of birds at the time fish eggs and larvae are present to evaluate this interaction.

Environmental Influence on Predation and Competition Between Marine Birds and Commercial Fish

Because fish are cold-blooded animals, temperature, through its influence on the rate of metabolism, is a major variable in determining the amount of energy needed for maintenance and for performing such essential activities as swimming and feeding—fish are less active, feed less, and grow more slowly in cold waters. For example, growth in young sockeye salmon is very slow at temperatures lower than 4°C (Donaldson and Foster 1941), and temperature profoundly affects their swimming speed (Brett et al. 1958). The rates of development of the eggs of some flatfish are closely correlated with water temperature (Ketchen 1956)—flatfish developed more rapidly at higher temperatures (Fig. 8). At lower temperatures, the rate of growth is also slower and, therefore, the duration of pelagic larval life is longer for demersal fish and shellfish.

Variations in sea temperature should, therefore, influence the extent to which fish are vulnerable to predation and competition. For example, eggs would take a longer time to hatch in colder than in warmer sea water. In both pelagic fish such as herring, whose eggs are laid in the intertidal zone, and in demersal fish with pelagic eggs such as the sole, the period of vulnerability of eggs to bird predation would be extended. At lower temperatures the length of the pelagic life of demersal fish and shellfish and their vulnerability to predation would also be greater than at higher temperatures. For example, the number of days between molts of the zoeal stages of snow crabs is temperature-dependent—the warmer the water, the less the time between molts (Kon 1970).

Fig. 7. Distribution and numbers of birds observed in Bristol Bay along seaward migration route of sockeye salmon (from Bartonek and Gibson 1972).

Temperature, through its effects on swimming speed, feeding activity, and growth of juvenile fish, might influence the magnitude of predation by birds on pelagic fish in the following ways: (1) lower sea temperatures would increase the vulnerability of juvenile fish to bird predation because swimming speed would decrease, and the time the fish are of a size that could be eaten by would-be predators would increase; (2) lower sea temperatures would reduce the feeding by fish and decrease the competition by fish for food exploited by birds; and (3) higher sea temperatures would have the opposite effect—the feeding by fish would increase consumption of the foods that birds feed on.

In the eastern Bering Sea, water temperatures may vary greatly between years for the same month (Fig. 9). Such variation should result in variation in the temperature-dependent activities of fish and, in turn, in magnitude of marine bird predation and competition.

Fig. 8. The relation of temperature to the rate of development to hatching of lemon sole, as compared with two European flatfishes (Ketchen 1956).

Possible Influences of Man on the Interaction of Marine Birds with Commercial Fish

We have noted that the abundance and age and size composition of major stocks of fish in the Bering Sea have been drastically reduced by commercial fishing. This has resulted in the reduction in numbers of fish at all life history stages, including those on which marine birds and other fishes depend for food. What effect this reduction has had on the abundance and distribution of marine birds in the Bering Sea is unknown. It depends in part on the ability of birds to eat other fish or increase their use of zooplankton or nekton.

We can hypothesize on probable changes in bird and fish abundance that resulted from the heavy commercial harvest of fish but any such changes cannot be documented or quantified. A reduction in stocks of a fish species could result in a reduced supply of food for a species of bird and cause a shift in the diet of this bird to other species of fish or to more zooplankton. For a bird species with specific food preferences, this could mean a reduction in its abundance to a level supportable by the available food supply. For bird species with less specific food requirements, a reduction in a species of fish could mean a reduction in competition for food with that fish—which could increase survival of the birds.

Man's intentional harvest of marine birds, such as the shearwater in parts of the southern hemisphere, and his inadvertent harvest of other bird species which are entangled or caught in fishing gear reduce predation and competition by marine birds. This, in turn, may aid the survival of the fish stocks in the Bering Sea.

The status of most stocks of commercial fish and shellfish in the Bering Sea is such that reductions in harvest are warranted, have been proposed, or are in effect. If the 200-mile (61-km) limit of jurisdiction over the marine resources by adjacent coastal States is implemented, either as a result of the Law of the Sea Conferences or unilaterally by the United States, we can expect commercial fishing in the eastern Bering Sea to be more tightly regulated. Such action should result in a reduction in harvest of those fish species now in a depleted condition, which, in turn, could influence the abundance of marine birds. Now is an opportune time to implement the studies required to increase our knowledge of the abundance, distribution, and seasonal movements of marine birds and their relationship to commercial fish resources of the eastern Bering Sea.

Conclusions

• The eastern Bering Sea is a region of high biological productivity; it is one of the world's great producers of commercial fish and major congregating areas for marine birds.

• The vulnerability of fish to predation by marine birds depends on life history features, such as place of spawning, duration of larval stages, growth rate, sea temperature, and adult size of fish, and on the distribution, feeding behavior, and food habits of marine birds.

Fig. 9. Sea temperatures in Bristol Bay and southeastern Bering Sea in mid-June and early July of 1967 and 1971 (from Straty 1974).

• The most apparent predation by marine birds on fish is on fish large or mature enough that some hard body parts persist and can be found in the stomach samples of birds.

• Little is known of the extent of bird predation on the pelagic eggs and larvae of demersal fish and shellfish in the Bering Sea because of lack of investigation and the rapid digestion of eggs and larvae by birds.

• Predation by marine birds on juvenile salmon is not well documented because of the lack of investigation in areas where both birds and fish are present.

• Marine birds and commercial fish eat similar zooplankton and fish in the eastern Bering Sea. The food exploited by both generally reflects the relative abundance of the types of food in the area, but food preference is displayed by some species of fish and birds.

• More is known about the food habits of the commercial fish than of the marine birds of the Bering Sea.

• Sea water temperature may be a major environmental factor in the Bering Sea since it influences both the extent to which fish are vulnerable to predation and the amount of competition with marine birds. Sea temperatures may vary greatly from year to year in the Bering Sea, and this may result in variations in the magnitude of predation and competition between birds and fish.

• The distribution of marine birds and the various stages in the life history of commercial fish are not well known for the eastern Bering Sea. Where these have been studied, they are intimately related. Such knowledge is required to gain some insight into even the potential for predation and competition in the dynamics of the marine bird and commercial fish populations of this region. In two instances, it is known that the occurrence of marine birds and the early life history stages of fish coincide so as to result in both potential predation on the fish by the birds and competition for food between the fish and the birds.

• The possibility exists that the commercial fish resources of the eastern Bering Sea will eventually come under the jurisdiction of the United States. This could mean reduced harvests of fish to restore depleted stocks. Such action could result in changes in the abundance of the marine birds of this region by creating an increased food supply for some and decreased supply for others.

Acknowledgments

We thank J. C. Bartonek and H. R. Carlson, H. Jaenicke, H. Larkins, and B. L. Wing for supplying various materials presented in this paper.

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