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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 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.

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:

• Secondary producers
• Zooplankton and micronekton
• Copepods
• Calanus spp.
• Eucalanus spp.
• Euphausiids
• Thysanoessa spp.
• Amphipods
• Parathemisto spp.
• Gammarus spp.
• Pteropods
• Spiratella spp.
• Clione spp.
• Chaetognaths
• Sagitta spp.
• Benthos
• Polychaetes
• Nereis spp.
• Euroe spp.
• Molluscs
• Mytilus edulis
• Tonicella spp.
• Fusitriton oregonensis
• Echinodermata
• Strongylocentrotus spp.
• Crustacea
• Gammaridae
• Mysidae
• Idothea spp.
• Pagurus spp.
• Hapalogaster spp.
• Sclerocrangon spp.
• Intermediate carnivores
• Eggs (littoral, adhesive)
• Clupeidae
• Pelagic larvae
• Gadidae
• Pleuronectidae
• Osmeridae
• Ammodytidae
• Salmonidae
• Gadidae
• Pandalidae
• Juvenile and small adults
• Clupeidae
• Osmeridae
• Ammodytidae
• Salmonidae
• Gadidae
• Pandalidae
• Large adults
• Clupeidae
• Gadidae
• Pleuronectidae
• Salmonidae
• Scorpaenidae
• Lithodidae
• Majidae
• Pandalidae
• Marine birds
• Alcidae
• Procellariidae
• Laridae
• Phalacrocoracidae

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.

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.

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).

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.

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.