Part II

: Review of other estimates. Bird-Banding 34:139-159.

Nisbet, I. C. T. 1973. Courtship feeding, egg-size and breeding success in common terns. Nature (Lond.) 241:141-142.

Orians, G. H. 1961. The ecology of blackbird _(Agelaius)_ social systems. Ecol. Monogr. 31:285-312.

Orians, G. H. 1969. Age and hunting success in the brown pelican _(Pelecanus occidentalis)_. Anim. Behav. 17:316-319.

Orians, G. 1971. Ecological aspects of behavior. Pages 513-546 _in_ D. S. Farner and J. R. King, eds. Avian biology. Vol. I. Academic Press, New York.

Parsons, J. 1970. Relationship between egg size and post-hatching chick mortality in the herring gull _(Larus argentatus)_. Nature (Lond.) 228:1221-1222.

Payne, R. B. 1965. The molt of breeding Cassin auklets. Condor 67:220-228.

Payne, R. B. 1972. Mechanisms and control of molt. Pages 103-155 _in_ D. S. Farner and J. R. King, eds. Avian biology. Vol. II. Academic Press, New York.

Pearson, T. H. 1968. The feeding biology of sea-bird species breeding on the Farne Islands, Northumberland. J. Anim. Ecol. 37:521-552.

Pennycuick, C. J. 1960. Gliding flight of the fulmar petrel. J. Exp. Biol. 37:330-338.

Porter, W. P., and D. M. Gates. 1969. Thermodynamic equilibria of animals with environment. Ecol. Monogr. 39:227-244.

Potts, G. R. 1968. Influence of eruptive movements, age, population size and other factors on the survival of the shag. J. Anim. Ecol. 37:53-102.

Potts, G. R. 1971. Moult in the shag _Phalacrocorax aristotelis_, and the ontogeny of the "Staffelmauser." Ibis 113:298-305.

Preston, F. W., and E. J. Preston. 1953. Variation of the shapes of birds eggs within the clutch. Ann. Carnegie Mus. 33:129-139.

Preston, W. C. 1968. Breeding ecology and social behavior of the black guillemot, _Cepphus grylle_. Ph.D. Thesis. Univ. of Michigan, Ann Arbor.

Pulliam, H. R. 1974. On the theory of optimal diets. Am. Nat. 108:59-74.

Richardson, F. 1961. Breeding biology of the rhinoceros auklet on Protection Island, Washington. Condor 63:456-473.

Ricklefs, R. E. 1968. Patterns of growth in birds. Ibis 110:419-451.

Ricklefs, R. E. 1973. Patterns of growth in birds. II. Growth rate and mode of development. Ibis 115:177-201.

Ricklefs, R. E. 1974. Energetics of reproduction in birds. Pages 152-292 _in_ R. A. Paynter, ed. Avian energetics. Publ. Nuttall Ornithol. Club 15.

Royama, T. 1970. Factors governing the hunting behavior and selection of food by the great tit _(Parus major L.)_. J. Anim. Ecol. 39:619-668.

Schamel, D. L. 1974. The breeding biology of the Pacific eider (_Somateria mollissima v-nigra_ Bonaparte) on Barrier Island in the Beaufort Sea, Alaska. M.S. Thesis. Univ. of Alaska, Fairbanks.

Schartz, R. L., and J. L. Zimmerman. 1971. The time and energy budget of the male dickcissel _(Spiza americana)_. Condor 73:65-76.

Schmidt-Nielsen, K. 1972. Locomotion: energy cost of swimming, flying, and running. Science 177:222-228.

Schoener, T. 1971. Theory of feeding strategies. Annu. Rev. Ecol. Syst. 2:369-404.

Schönwetter, M. 1967. Handbuch der oologie. Vol. I. Akademie-Verlag, Berlin.

Sealy, S. G. 1973_a_. Breeding biology of the horned puffin on St. Lawrence Island, Bering Sea, with zoogeographical notes on the North Pacific puffins. Pac. Sci. 27:99-119.

Sealy, S. G. 1973_b_. Adaptive significance of post-hatching developmental patterns and growth rates in alcidae. Ornis Scand. 4:113-121.

Sealy, S. G. 1975_a_. Feeding ecology of the ancient and marbled murrelets near Langara Island, British Columbia. Can. J. Zool. 53:418-433.

Sealy, S. G. 1975_b_. Aspects of the breeding biology of the marbled murrelet in British Columbia. Bird-Banding 46:141-154.

Sealy, S. G. 1975_c_. Influence of snow on egg-laying in auklets. Auk 92:528-538.

Smith, C. R. 1973. Time budget of the loggerhead shrike in southwest Florida. Abstracts of papers presented to the Wilson Society meeting, Cornell University.

Smith, N. G. 1966. Evolution of some arctic gulls _(Larus)_: an experimental study of isolating mechanisms. Am. Ornithol. Union Monogr. 4. 99 pp.

Snow, B. K. 1960. The breeding biology of the shag _Phalacrocorax aristotelis_ on the Island of Lundy, Bristol Channel. Ibis 102:554-575.

Snow, B. K. 1963. The behaviour of the shag. Br. Birds 56:77-103; 164-186.

Southern, W. E. 1967. Dispersal and migration of ring-billed gulls from a Michigan population. Jack-Pine Warbler 45:102-111.

Spaans, A. L. 1971. On the feeding ecology of the herring gull _Larus argentatus_ Pont. in the northern part of the Netherlands. Ardea 59:73-189.

Speich, S., and D. A. Manuwal. 1974. Gular pouch development and population structure of Cassin's auklet. Auk 91:291-306.

Stiles, F. G. 1971. Time, energy and territoriality of the Anna hummingbird _(Calypte anna)_. Science 173:818-821.

Storer, R. W. 1952. A comparison of variation, behaviour and evolution in the seabird genera _Uria_ and _Cepphus_. Univ. Calif. Publ. Zool. 52:121-222.

Storer, R. W. 1960. Evolution in the diving birds. Proc. Int. Ornithol. Congr. 12(Vol. II):694-707.

Stresemann, E., and V. Stresemann. 1966. Die Mauser der Vögel. J. Ornithol. 107 (suppl.):1-448.

Thoresen, A. C. 1964. The breeding behavior of the Cassin auklet. Condor 66:456-476.

Tinbergen, N. 1935. Field observations of east Greenland birds. I. The behaviour of the red-necked phalarope (_Phalaropus lobatus_ L.) in spring. Ardea 24:1-42.

Tinbergen, N. 1960. The herring gull's world. Basic Books, Inc., New York.

Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136-179 _in_ B. Campbell, ed. Sexual selection and the descent of man, 1871-1971. Aldine-Atherton, Chicago, Illinois.

Tschanz, B. 1959. Zur brutbiologie der trottellumme (_Uria aalge aalge_ Pont.). Behaviour 14:1-100.

Tuck, L. 1960. The murres. Canadian Wildlife Service Series 1. 260 pp.

Tucker, V. A. 1969. The energetics of bird flight. Sci. Am. 220(5):70-78.

Tucker, V. A. 1970. Energetic cost of locomotion in animals. Comp. Biochem. Physiol. 34:841-846.

Tucker, V. A. 1972. Metabolism during flight in the laughing gull, _Larus atricilla_. Am. J. Physiol. 222:237-245.

Tucker, V. A. 1974. Energetics of natural flight. Pages 298-328 _in_ R. A. Paynter, Jr., ed. Avian energetics. Publ. Nuttall Ornithol. Club 15.

Utter, J. M., and E. A. LeFebvre. 1970. Energy expenditure for free flight by the purple martin _(Progne subis)_. Comp. Biochem. Physiol. 35:713-719.

Utter, J. M., and E. A. LeFebvre. 1973. Daily energy expenditure of purple martins _(Progne subis)_ during the breeding season: Estimates using D₂O¹⁸ and time budget methods. Ecology 54:597-604.

Verbeek, N. A. M. 1964. A time and energy budget of the Brewer blackbird. Condor 66:70-74.

Verbeek, N. A. 1972. Daily and annual time budget of the yellow-billed magpie. Auk 89:567-582.

Vermeer, K. 1963. The breeding ecology of the glaucous-winged gull _(Larus glaucescens)_ on Mandarte Island, B. C. B. C. Prov. Mus. Occas. Pap. 13:1-104.

Verner, J. 1965. Time budget of the male long-billed marsh wren during the breeding season. Condor 67:125-139.

Ward, J. G. 1972. Studies on the feeding ecology and breeding success of the glaucous-winged gull _(Larus glaucescens)_ on Mandarte and Cleland Islands. Ph.D. Thesis. Univ. of British Columbia, Vancouver.

Weaver, D. K. 1970. Parental behavior of the herring gull _(Larus argentatus smithsonianus)_ and its effect on reproductive success. Ph.D. Thesis. Univ. of Michigan, Ann Arbor.

West, G. C. 1967. Nutrition of tree sparrows during winter in central Illinois. Ecology 48:58-67.

Wilbur, H. M., D. W. Tinkle, and J. P. Collins. 1974. Environmental certainty, trophic level, and resource availability in life history evolution. Am. Nat. 108:805-817.

Williams, G. C. 1966. Adaptation and natural selection. Princeton Univ. Press, Princeton, N. J.

Willson, M. F. 1971. Seed selection in some North American finches. Condor 73:415-429.

Willson, M. F., and J. C. Harmeson. 1973. Seed preferences and digestive efficiency of cardinals and song sparrows. Condor 75:225-233.

Wolf, L., and F. R. Hainsworth. 1971. Time and energy budgets of territorial hummingbirds. Ecology 52:980-988.

Zar, J. H. 1968. Standard metabolism comparisons between orders of birds. Condor 70:278.

FOOTNOTES:

[41] Common eider, 2 to 7 h.

[42] No data given.

[43] Indirect evidence that young are brooded this long.

[44] Data from Lack (1968) and Ashmole (1971) unless otherwise noted.

[45] Cullen (1957).

[46] Birkhead (1974).

[47] Speich and Manuwal (1974).

Zoogeography and Taxonomic Relationships of Seabirds in Northern North America

by

M. D. F. Udvardy

California State University Sacramento, California 95819

Abstract

The zoogeography and taxonomic relationships among 42 living and 1 extinct species of marine birds from the northern and northwestern coasts of North America are described. Seventeen species are circumpolar in distribution; 17 are endemic to Beringia, and 8 have origins in the North Pacific.

This discussion concerns the northern and western coasts of the continent, from about the Mackenzie Delta westward and southward to the mouth of the Columbia River. Besides bona fide seabirds, I include marine birds that predominantly breed and feed on or around the marine littoral, but exclude two groups: shorebirds, jaegers, and phalaropes, which breed inland and move out from the Arctic after an undetermined postbreeding period; and Anseriformes which become "marine birds" in their southern winter quarters. What remains is 42 living species (Table 1).

The Procellariiformes, or tube-nosed seabirds, have a predominantly southern hemispheric, Gondwanan distribution. The North Pacific basin is an important feeding ground of several shearwaters (_Puffinus_ spp.) that breed in the South Pacific and subantarctic. Only three species breed in the area under consideration: the fulmar _(Fulmarus glacialis)_ and two storm-petrels (_Oceanodroma_ spp.), all of which are still relatively widespread.

Of the Pelecaniformes, the very successful, worldwide cormorants (_Phalacrocorax_ spp.)--inland water as well as coastal and "amphibious" species are on every continent--are ancient Pacific dwellers, with a high grade of endemism here: Of the two subarctic species, one _(P. perspicillatus)_ became extinct long ago, and the other, the red-faced cormorant _(P. urile)_, is very restricted, and deserves our greatest attention. The pelagic cormorant _(P. pelagicus)_, Brandt's cormorant _(P. penicillatus)_, and the double-crested cormorant _(P. auritus)_ are widespread and successful, extending south of the area here considered; double-crested cormorants also breed inland and across toward the North Atlantic coast. As fish-eaters they are often persecuted where coastal fishermen possess firearms, and thus are sensitive to increasing human influence on the coasts.

Two species of arctic geese need special attention. The emperor goose _(Philacte canagica)_ is a Beringean endemic and lives in a very restricted area of both sides of this sea; its status (endangered?) is unknown to me. Since the black brant _(Branta bernicla)_ is a long-range migrant, it is hunted as a game bird at its winter grounds, and subject to management measures. Whereas the emperor goose is a unique offshoot of the genus Anser, the Pacific brant is considered a subspecies; its general distribution is circumpolar.

Five arctic ducks, and one other, constitute the sea ducks of the area. The common eider _(Somateria mollissima)_, king eider _(S. spectabilis)_, and the oldsquaw _(Clangula hyemalis)_ are widespread, and circumpolar or nearly so; hunting and down-robbing in other parts of the Arctic may provide clues as to their relative tolerance of primitive or advanced civilization. The spectacled eider _(S. fischeri)_ and Steller's eider _(Polysticta stelleri)_ are restricted to the Bering Sea coasts and neighboring High Arctic coasts, respectively; their status is precarious.

Table 1. _Seabirds in northwestern North America._ (x = breeding, w = wintering or transient, () = either scarce or restricted distribution, * = stragglers only, nesting status unclear)

Distribution --------------------------------------------- |Circumpolar | |Widespread in North Pacific | | |North coast of Alaska | | | |Beringia[48] | | | | |Aleutian Islands | | | | | |South coast of Alaska[49] | | | | | | |Temperate northeast Species | | | | | | |Pacific coast[50] _Fulmarus glacialis_ x w x x x w _Oceanodroma furcata_ x x x x _O. leucorhoa_ x x x x x _Phalacrocorax auritus_ x x x _P. penicillatus_ (x) x _P. pelagicus_ x x x x x _P. urile_ x x x _Branta bernicla_ x x x (w) (w) w _Anser canagicus_ x w w _Clangula hyemalis_ x w x x w w w _Histrionicus histrionicus_ x w w w w w _Polysticta stelleri_ x x (w) _Somateria mollissima_ x x x x x _S. spectabilis_ x x x w (w) _S. fischeri_ x x _Larus hyperboreus_ x w x x w w w _L. glaucescens_ x x x x _L. occidentalis_ (x) _L. argentatus_ x w x (x)w _L. thayeri_ w x w w w w _L. canus_ x w x x (x)w _Rissa tridactyla_ x w x x x x w _R. brevirostris_ x x (x) _Xema sabini_ x x x w _Sterna paradisaea_ x w x x x w _S. aleutica_ x x _Uria aalge_ x x (x) x x x x _U. lomvia_ x x x x x x _Alle alle_ x * _Cepphus grylle_ x x w _C. columba_ x x x x x _Brachyramphus marmoratus_ x (x) x x _B. brevirostris_ x x x _Synthliboramphus antiquus_ x x x x x _Ptychoramphus aleuticus_ x x x _Cyclorrhynchus psittacula_ x x _Aethia cristatella_ x x _A. pusilla_ x x _A. pygmaea_ x _Cerorhinca monocerata_ x x x _Fratercula corniculata_ x x x x x _Lunda cirrhata_ x x x x x Total number of nesting species 17 11 15 27 25 24 17 Total number of wintering species 9 4 7 9 9 Grand total 17 20 15 31 32 33 26

The harlequin duck _(Histrionicus histrionicus)_ stands alone without close relatives. It often breeds far from the sea, but spends the shortest time--only a few weeks--away from the rocky coast. There is a year-round population of yearlings in the sea. The drakes of the nearest breeding pairs at lower latitudes are back to the sea, abandoning their mates at the breeding stream when the alpine stream-dwellers are still at sea awaiting the thawing of their breeding grounds. Harlequin ducks live in large parts of Siberia, from arctic Alaska to central California and Colorado, and also in the eastern Arctic. They do not seem to me to be in immediate danger globally, though perhaps they are locally.

Gulls are a highly successful group of seabirds, and of the eight species on our coasts the four more southern ones--the western gull _(Larus occidentalis)_, glaucous-winged gull _(L. glaucescens)_, common gull _(L. canus)_, and herring gull _(L. argentatus)_--are expanding wherever civilization creates new scavenging opportunities. Nothing is said about the populations of the kittiwake _(Rissa tridactyla)_, black-legged kittiwake _(R. brevirostris)_ and Sabine's gull _(Xema sabini)_, or of the other two high arctic species (_Pagophila eburnea_, _Rhodostethia rosea_) which do not nest regularly in the area considered here.

The arctic tern _(Sterna paradisaea)_ is circumpolarly widespread and successful, whereas the Aleutian tern _(S. aleutica)_ is a very restricted Beringean endemic, and its status needs to be exactly known.

Almost one-third of the seabirds in this area are alcids, a family centered in the North Pacific and, more specifically, in the Bering Sea. Most species breed in enormous rookeries. Any impact of civilization is highly detrimental under such circumstances. Of the four circumpolar species the two _Uria_ guillemots (murres) are important. The dovekie _(Alle alle)_ is a sparse pioneer of Bering Strait, as is the black guillemot _(Cepphus grylle)_ on our side of the Arctic Sea. Its congener, the pigeon guillemot _(C. columba)_, is common and successful all the way to coastal central California. Of the remaining 11 species, special attention should be paid to the whiskered auklet _(Aethia pygmaea)_ of the Aleutian chain; the Kittlitz's murrelet _(Brachyramphus brevirostris)_ of the eastern Beringean and southern Alaska coast; and to the widespread, but very sporadic rhinoceros auklet, or puffin _(Cerorhinca monocerata)_.

To sum up, I have tabulated these 42 species, and indicated whether modern life-history and population studies are extant:

No. No. species studied

Procellariiformes 3 2 _Phalacrocorax_ 4 2 Anseres 2 1 Anates 6 -- Lari 9 2 Sterni 2 -- Alcidae 16 7 Total 42 14

Thus, 28 species await studies preliminary to, and highly necessary for, conservation measures.

Seventeen species of marine birds are spread either circumpolarly around the northern perimeter or along the north-south coasts of the Laurasian continents. Four of these are of the High Arctic (_Branta bernicla_, _Somateria spectabilis_, _Xema sabini_, _Alle alle_); another seven penetrate the Bering Sea as well (_Fulmarus glacialis_, _Somateria mollissima_, _Clangula hyemalis_, _Larus hyperboreus_, _Rissa tridactyla_, _Sterna paradisaea_, _Uria lomvia_); and six are panboreal-subboreal, widespread in their distribution--_Oceanodroma leucorhoa_ (extends far south), _Histrionicus histrionicus_, _Larus argentatus_ (widespread latitudinally), _L. canus_ (also inland), _Uria aalge_, and _Cepphus grylle_.

Seventeen species of marine birds are endemic to Beringia: _Anser canagicus_, _Polysticta stelleri_, _Somateria fischeri_, _Rissa brevirostris_, and _Aethia pusilla_ (and the extinct _Phalacrocorax perspicillatus_); _P. urile_, _Sterna aleutica_, _Aethia pygmaea_, _A. cristatella_, and _Cyclorrhynchus_ extend westward to the Sea of Okhotsk, as do _Brachyramphus brevirostris_ and _Larus glaucescens_, which also extend eastward; and _Phalacrocorax pelagicus_, _Cepphus columba_, _Fratercula corniculata_, and _Lunda cirrhata_ are amphipacific species in Beringia.

Eight species of marine birds are associated with the North Pacific. Four are found on both sides of the ocean--_Oceanodroma furcata_, _Brachyramphus marmoratus_, _Synthliboramphus antiquus_, and _Cerorhinca monocerata_ (very disjunct). The four others occur on only the North American side--_Phalacrocorax auritus_ (also inland), _P. penicillatus_, _Larus occidentalis_ (albeit barely), and _Ptychoramphus aleuticus_.

Finally, one species, _Larus thayeri_, is endemic at the central Canadian Arctic, extending westward into the area here considered.

FOOTNOTES:

[48] Beringia comprises the islands and coasts of the Bering Sea.

[49] South coast of Alaska extends from the tip of the Alaska Peninsula to Glacier Bay.

[50] Temperate northeast Pacific coast extends from Glacier Bay south to the mouth of the Columbia River.

CONFLICTS BETWEEN THE CONSERVATION OF MARINE BIRDS AND USES OF OTHER RESOURCES

Social and Economic Values of Marine Birds

by

David R. Cline[51] and Cynthia Wentworth

U.S. Fish and Wildlife Service Anchorage, Alaska

and

Thomas W. Barry

Canadian Wildlife Service Edmonton, Alberta, Canada

Abstract

Throughout history, marine birds have provided tangible and intangible benefits to human societies. Unregulated exploitation of some species by explorers, mariners, and colonists led to the extinction of the great auk _(Pinguinus impennis)_ and near extinction of others, including the Bermuda petrel _(Pterodroma cahow)_ and the North Pacific albatrosses (_Diomedea_ spp.). Marine birds continue to provide commercial, subsistence, recreational, scientific, and educational values to people of many nations, while playing critical roles in the economies of the world's oceans.

Annual harvest of slender-billed shearwaters _(Puffinus tenuirostris)_ known as "muttonbirds" in Australia, sooty tern _(Sterna fuscata)_ eggs in the Caribbean, murres (_Uria_ spp.) and eiders (_Somateria_ spp.) in Greenland and the Soviet Union, and guano in Peru and Africa represent the principal commercial uses of marine birds and their products. Residents of the Faeroes Islands and thousands of native people in Greenland and arctic Canada and Alaska use various species for subsistence. The annual rituals of bird hunting and egg gathering are deeply ingrained in the sociocultural traditions of these peoples and continue to be important to their social welfare.

Most countries of the world are currently providing at least some protection to their marine bird resources. However, the destruction of bird habitats by man's developments and the contamination of marine environments by industrial pollutants are posing increasingly serious threats to many species. If managed and used in accordance with scientific principles of sustained yield, some of the more abundant species of marine birds can continue to provide long-term social and economic benefits to man.

Increasing numbers of people are expending considerable sums of money to reach marine bird viewing areas off the coasts of North American States and Provinces. Preliminary evidence indicates such nonconsumptive pursuits are contributing significant amounts of money to regional economies and helping businessmen earn a living. An accurate evaluation of both biological and economic impacts resulting from these nonconsumptive activities is urgently needed.

The possibility of establishing an excise tax on designated outdoor recreational equipment appears to hold considerable potential for more adequately funding marine bird programs, as well as those for other nongame wildlife.

Greater citizen involvement in sociopolitical processes will, to a large extent, determine the success of marine bird conservation programs. Sound conservation legislation that insures adequate protection of habitat and provides for enlightened and innovative thrusts in conservation, education, research, management, and law enforcement will help insure the survival of all species of marine birds and, in turn, provide social and economic benefits to people across generations. #/

In its 17 March 1975 issue, _Time_ magazine reported battalions of observers from all over the country flocking to Salisbury, Massachusetts, armed with telescopes, cameras dwarfed by huge telephoto lenses, sketch pads, and binoculars. There, 1,500 strong the first weekend alone, they took up vigil along the seawall of the Merrimack River. A local businessman circulated among the chilly bird-watchers with free coffee and hot chocolate, while handing out a pamphlet advertising his restaurant.

The cause of the commotion was the appearance of a single, unassuming, pigeon-like seabird called a Ross' gull _(Rhodostethia rosea)_, almost never seen south of the Arctic Circle and never before in the contiguous 48 States. Time stated that "for those who care about such matters the event was as electrifying as the descent of a Martian spaceship."

Meanwhile, far above the Arctic Circle at Point Barrow on the Arctic Ocean, Eskimo hunters probably puzzled at the strange ways of the white "birdmen," as they recalled the savory dishes Ross' gulls provided many of them during the previous fall hunting season. This particular gull is considered a delicacy by the Eskimos, and the birds are actively sought each year as they fly near shore during their fall wanderings from Asian breeding grounds.

Perhaps this dichotomy of people's interests in a single species is indicative of the broad spectrum of social and economic values man derives from marine birds. Perhaps, too, it represents the challenge that wildlife professionals, administrators, and citizen conservation leaders face in today's complex world in striving to sort out priorities in allocation of such common property (amenity) resources among beneficial users.

As with the Ross' gull, socioeconomic values of marine birds involve both consumptive and nonconsumptive uses. Consumptive uses may provide socioeconomic values in the form of meat, eggs, oil, feathers, down, and guano. Cultural and recreational benefits may also be involved. Nonconsumptive uses benefit the tourist and recreation industries as well as providing less tangible social values, such as esthetic appreciation and environmental education and scientific study opportunities.

In this paper we examine some social and economic indicators that are believed to demonstrate people's growing awareness and interest in marine birds. These indicators involve a broad spectrum of values and illustrate the critical need for adoption of a strong North American marine bird conservation program.

Historical Perspective

Since earliest times, marine birds have accompanied the evolution of human societies in coastal and insular environments of the world. Their social value is in part recorded in kitchen middens of ancient campsites and villages. From the time man first inhabited the seacoasts and ventured out in ships, the company of seabirds has added life and inspiration to what otherwise would be a bleak and desolate landscape. Fishermen long ago learned to use seabirds to show them where the rich fishing grounds were located, and the cries of birds were often used to guide mariners away from dangerous cliffs during foggy weather.

At the time of the first contact with Europeans, native peoples of arctic Canada and Alaska reportedly took birds with bolas, snares, spears, arrows, and nets; they herded flightless waterfowl and gathered eggs as well. Brandt (1943) said that Alaskan Eskimos would have been destitute if eiders (_Somateria_ spp.) had not been available for food and clothing, and Ekblaw (1928) believed the dovekie _(Plautus alle)_ saved the polar Eskimo from extinction.

Marine birds have often served as an emergency food supply for explorers, sailors, and others: according to Tuck (1960) "The accounts of early arctic explorers and marooned whalers describe many instances in which starvation was averted by eating murres" (_Uria_ spp.). One burrowing petrel of Australia was given the title "the bird of providence" because it saved the lives of shipwrecked mariners and convicts when supply ships from Sydney failed to reach them between March and August of 1790 (Serventy 1958).

Marine birds have also been taken because of the economic values of their feathers and oil. When economic overutilization has occurred, entire species were sometimes totally destroyed. This in fact happened to the great auk _(Pinguinus impennis)_. When Jacques Cartier visited the Funk Islands off Newfoundland in May 1534, he and his crew filled several barrels with great auks and salted them down for future consumption. So severe was the slaughter in the next 3 centuries that the species became extinct in its known breeding haunts, which originally extended from Newfoundland through Greenland and Iceland, to the Hebrides. The last one was killed at a stack rock off Iceland in 1884 (Lockley 1973).

Other species have been almost totally destroyed. Colonization of Bermuda by Spain in the 17th century resulted in the near annihilation of the Bermuda petrel _(Pterodroma cahow)_ there. Ships' crews found the birds to be fat and delicious, and they dried and salted those that could not be eaten fresh. Today, only about 20 breeding pairs remain, and are under strict protection by the Bermudan government (Lockley 1973).

The North Pacific albatrosses (_Diomedea_ spp.) were nearly exterminated by Japanese feather hunters near the end of the 18th century. The short-tailed albatross _(D. albatrus)_ was also nearly wiped out at its breeding colonies west of the Hawaiian Islands (Bourne 1972).

Other species that were carelessly exploited for their meat and plumage in the past, but which have since regained their numbers, include the fulmar _(Fulmarus glacialis)_ on St. Kilda Island in the North Atlantic; and the North Atlantic, South African, and Australian gannets (_Morus bassanus_, _M. capensis_, and _M. serrator_) (Bourne 1972; Lockley 1973). In some instances entire breeding colonies of a species have been destroyed while others have survived. On the Abrothos Islands in western Australia, for example, large nesting colonies of sooty terns _(Sterna fuscata)_ and common noddies _(Anous stolidus)_ appear to have been wiped out on Rat Island by indiscriminate "egging" for food, whereas similar-sized colonies survive on other islands, where they are now controlled by the Fisheries and Fauna Department (Serventy et al. 1971).

Historically, it has probably been man's unregulated harvest of marine birds that has been the primary cause of their destruction. Generally, the loss of a species because of unregulated harvest is no longer a matter of major concern, because most countries of the world are providing at least some protection for their marine birds. However, other factors such as habitat destruction and contamination of the marine environment by industrial pollutants are posing increasingly serious threats to many.

Social and Economic Indicators

Economic indicators concerning consumptive uses of wildlife, including marine birds, are frequently misunderstood. In a dollar-oriented and over-consumptive society like ours, economic values are usually seen as being in conflict with esthetic values. "Economic use" usually conjures up images of man's overutilization and, hence, long-term depletion of wildlife resources. However, when speaking of economic use, it is important to distinguish between such overuse and sustained-yield management.

Although both types of use have provided economic benefits over the years, overharvest that results in long-term resource depletion is not usually the most or best economic use in the long run; obviously a "harvest" cannot be sustained at a given level when the resource base is constantly being depleted. On the other hand, when certain species of marine birds are used in accordance with principles of sustained yield, they can provide long-term economic values to society in conjunction with the social, esthetic, and intangible values that their preservation insures. Of course, for many species esthetic values far outweigh economic ones derived through commercialization.

_Commercial Uses_

Muttonbirds

The muttonbird industry of Australia is an excellent example of the commercial use of marine birds on a sustained-yield basis. Fledgling Tasmanian muttonbirds, or slender-billed shearwaters _(Puffinus tenuirostris)_, are commercially harvested each year from their colonies on islands of Bass Strait, mainly in the Flinders Island group.

These muttonbirds are marketed as fresh or salted "Tasmanian squab." Various by-products, including oil, body fat, and feathers, are also sold. In 1968, a total of just under one-half million young birds were taken. Prices to the producers varied from $12 to $14 (Australian dollars) per hundred salted birds and $16 per hundred fresh birds. Stomach oil brought 75¢ per gallon. Assuming the average price per hundred birds to be $14, the meat alone was worth about $70,000 per year to the producers. The retail value was of course much higher. Although the muttonbird harvest is no longer the mainstay of the Flinders Island economy, according to Serventy (1969) it is still a picturesque and important annual social event.

Serventy et al. (1971) believed the commercialization of the muttonbird preserved its numbers: "Had there been no vested interests to preserve the 'birding islands' as such, many of them would in the course of time have been 'improved' as sheep stations and the shearwater populations would have declined and vanished."

Sooty Terns

The Caribbean is the home of the world's most important wild egg producer--the sooty tern. In some years about 2 million sooty tern eggs from the Seychelles and 0.6 million from Morant and Pedro bays have reached Caribbean markets (Tuck 1960).

Eiders and Murres

Although the shooting of birds is not as important economically to Greenland's approximately 50,000 residents as are sealing, whaling, and fox hunting, the harvest of seabirds is an ancient tradition that still means production of an important food source that the many Greenlanders could not exist without. About 30 species of marine birds are harvested for human consumption, eider ducks and murres being by far the most important. In west Greenland about 750,000 birds (equivalent to about 825 tons of meat) and 10,000 eggs are harvested annually. Murres constitute the main dish in summer at small coastal outposts with access to rookeries. Great quantities are also dried and salted for use in winter. Murre canneries at Upernavik have supplied southern cities with the frozen meat of about 25,000 to 30,000 murres annually. However, this commercial activity would be prohibited by a proposed new Greenland game law (Salomonsen 1970).

Banding has shown that about 22% of Greenland's eider population, or about 150,000 birds, is shot annually. Collecting of eider eggs is now prohibited except in the Thule District, where 10,000 are taken annually. Eider down is still collected from nests for sale to a trading company for the manufacture of much demanded eider-down coverlets (Salomonsen 1970).

A growing human population, the widespread use of modern firearms, and the increasing use of speedboats in hunting have resulted in serious declines in many of Greenland's marine bird populations. The Greenland government has demonstrated its concern by instituting protective measures in response to Danish expert advice. For example, the common puffin _(Fratercula arctica)_ was given 10 years of total protection in 1961 after bird numbers had seriously declined as a result of over-harvesting of the birds and their eggs (Lockley 1973). This protection was extended in 1970. Also, it is now illegal to discharge firearms at most marine bird rookeries in Greenland.

With protection of bird habitats from human intrusion and toxic environmental pollutants, adequate enforcement of sound conservation laws, greater efforts in conservation education, and scientific regulation of harvests, Greenland's valuable marine bird resource could probably withstand intensive utilization indefinitely (F. Salomonsen, personal communication). Salomonsen has been quick to point out, however, that people should not be encouraged to believe that the value of seabirds for food is the only reason they should be saved.

Although several species of marine birds serve as sources of food in the Soviet Union, down of eider ducks and eggs of murres are considered to be the most important to the economy. These birds are referred to as trade birds due to their commercial importance (Belopol'skii 1961).

Guano

Peruvian guano beds are currently being managed on a sustained-yield basis; the harvest, as in the days of the Incas, depends entirely on the amount of guano deposited each year. Conservation and management policies have resulted in a steady increase in the amount extracted, from around 20,000 tons in 1900 to over 200,000 tons in 1971 (Lockley 1973).

The islands off south and southwest Africa are also commercial producers of guano. The annual yield from these breeding colonies averaged 3,971 tons in the 12-year period, 1961-72. In 1969, guano brought 4.75 Rands (equivalent to $7.11) per 200-pound bag. South African gannets are apparently depositing guano that is worth twice as much as the fish they consume to produce it (Jarvis 1971).

_Indirect Commercial Benefits_

Marine birds also play significant roles in the economies of the world's oceans, where algae, invertebrates, fish, seabirds, mammals, and man interact in complex ways. The bioenergetics and nutrient cycling in ocean ecosystems is even less well understood than the contributions seabirds make to man's dollar economies.

Sanger (1972) has conservatively estimated that in the subarctic Pacific region alone, birds consume from 0.6 to 1.2 million tons of food and return from 0.12 million to 0.24 million tons of feces each year.

Marine bird excrement is especially rich in nitrates and phosphates, which phytoplankton, the basis of ocean food pyramids, requires. Marine birds then, at least to some extent, help to sustain the northern commercial, recreational, and subsistence fishing industries. The fisheries in turn sustain seals and certain other mammals which are also essential elements of northern subsistence and recreational economies. Thus, marine birds contribute economic benefits indirectly as well as directly by serving as critical links in ecosystem food chains (Tuck 1960).

_Subsistence Uses_

The use of marine birds and their products does not have to be commercial to be economic. Economics is the science of the allocation of scarce resources. Any resource, regardless of whether it is bought or sold, has value to people and is therefore an economic commodity. Thus, any society has an economy whether or not it uses cash, and when the meat, feathers, or oil of marine birds are used, the birds have economic value. The problem, of course, is that of trying to determine just what this value is when a cash medium does not exist.

One of the ways to estimate this value is to assign implicit gross dollar values to seabirds, based on what it would cost to replace products derived from them with store-bought items of a similar, or substitutable, nature (this is a gross rather than a net value because it does not include the cost of guns, ammunition, transportation, etc., required to harvest and process the resource).

There have been many occasions in the past when it would have been physically impossible to find substitutes for seabird products. In such cases, and where seabirds may well have meant the difference between life and death, the economic value of the resource could be considered a plus infinity.

There are probably few, if any, places in the world today where people would starve if they could not obtain marine birds. However, there are still many situations where available substitutes are poor, or very expensive. And there are others where, even though the birds are no longer necessary for economic survival, they are still very important in terms of sociocultural traditions. According to Tuck (1960), "Wherever a wild animal is important to the economy of a people, its capture and use become part of the tradition of that people." Thus, while economic values can be measured in terms of substitutable store-bought foods, social and cultural values cannot be. To force complete dependence on a people by flying in foods from "Outside" is often socially intolerable because it tends to remove pride, a sense of worth, and therefore the reasons for living.

Marine birds have served as important sources of food in the Faeroes Islands for centuries, the puffin being unquestionably the most valuable. Williamson (1945) reported that in a good year the total puffin catch may be between 400,000 and 500,000. In addition, as many as 120,000 murres are snared or shot annually by the Faeroese, and at least twice that many eggs are taken and Tuck (1960) stated, "The economic necessity of 'fowling' in the Faeroes has by virtue of long centuries of usage become part of the national life, affecting folklore and customs, and providing outlets for the sporting instinct inherent in the people." A Faeroese guidebook even suggests that its importance to the Faeroese culture has been in no way diminished by the influence of modern civilization. Current Faroese game laws appear to be effective in assuring a sustained yield of marine birds while guaranteeing their long-term survival.

Seabirds and their eggs constitute a small, but still very important, part of the total diet of the Eskimos and Indians living along the Arctic coast of the Northwest Territories and Alaska. In spite of the many changes occurring in the North, there is, even for the wage earner, a strong psychological attachment to the land and sea and the free life it represents. In spring, the release from the long monotonous winter is marked by the rites of ratting, fishing, sealing, whaling, or marine bird hunting and egg gathering, according to village tradition.

For those living off the land in such remote coastal outposts as Sachs Harbor on Banks Island, Holman Island on the Mackenzie Delta, Point Hope and Point Barrow in northern Alaska, Inalik on Diomede Island in the Bering Strait, or Hooper Bay on the Yukon-Kuskokwim Delta, the spring marine bird hunt represents a change of diet and activity. It offers opportunity to renew age-old traditions and continues a cultural bond among those confined to jobs in the settlements--vacationing and absenteeism from jobs and schools are always highest during late May and early June.

Marine birds yield between a few grams and 2 kg of meat, depending on the species. Usually the birds are either consumed soon after they are taken or stored in an icehouse for use throughout the summer. Most often the meat is cooked into a soup or stew with rice, noodles, and onions. A few birds may be dried or salted so that they can be used for special holiday feasts during the winter. Sometimes feathers are saved for the manufacture of parkas, ceremonial fans, and masks. In some areas of the Yukon Delta, goose and duck down is still saved and used in quilts that can be found in nearly every home. In the spring 1975 issue of the catalog of a Seattle, Washington, outfitter, down quilts for single beds were listed at $95. Thus, there is a substantial cash savings by home manufacture of such items.

The Yukon Delta in western Alaska is the area where the use of marine birds is most extensive and significant. Klein (1966) provided harvest data by village for the entire area and showed that, in general, geese were more important than ducks, representing about two thirds of the take in both the spring and the fall. The average numbers of ducks (mostly pintails, _Anas acutus_) and geese (primarily white-fronted geese, _Anser albifrons_); emperor geese, _Philacta canagica_; cackling Canada geese, _Branta canadensis minima_; and black brant, _Branta nigricans_, taken per household were 77 by the Yukon River villages, 69 by the Kuskokwim River and tundra villages, and 94 by the Bering Sea coastal villages. Although eggs gathered by Yukon River villagers averaged less than a dozen per household, Kuskokwim people took about 3 dozen and coastal people about 6.5 dozen on the average. Eggs of black brant and cackling Canada geese were especially favored, but even those of small passerines were acceptable. The average size of households for all areas was believed to be between 5.5 and 6.5 persons.

A 1968 survey of waterfowl taken in the Mackenzie Delta region, made by the Canadian Wildlife Service, showed an average take per household of about 70 birds, a figure comparable to that for the Yukon Delta. In the Mackenzie region, however, ducks were more important than geese, representing about 60% of the harvest.

More recent data on Alaska waterfowl harvest per household is available for other coastal regions. Data provided by two regional native corporations for the Joint Federal-State Land Use Planning Commission for Alaska in 1973 showed an average per-household waterfowl harvest of 33 ducks and geese for Kotzebue area villages, 68 for Norton Sound villages, 24 for northwest Seward Peninsula villages, and 37 for St. Lawrence, Diomede, and King Island villages.

A 1974 subsistence survey carried out jointly by the University of Alaska and the Bristol Bay Native Corporation showed that, in 20 Bristol Bay villages, 57% of the households harvested waterfowl. The average kill was 32 birds per household.

Eider ducks are the most important marine birds taken by residents of Barrow, Alaska. Johnson (1971) interviewed 31 adult hunters with average kills of 88 birds per hunter. Barrow people also take substantial numbers of geese at Atkasook, a summer camp on the Meade River 80 miles southeast of Barrow.

Point Hope, Alaska, villagers also favor eider ducks above all others. Pederson (1971) indicated that each household that hunted took about 150 eiders in the summer of 1971. Each summer, Point Hope and Kivalina residents travel to the Cape Thompson and Cape Lisburne cliffs to gather murre eggs. Both Pederson (1971) and Kessel and Saario (1966) showed an average harvest of 5 to 10 dozen eggs per household (equivalent in weight to 10 to 20 dozen chicken eggs).

To our knowledge, there is no available evidence to indicate that the number of migratory birds taken in the North in spring and fall is a significant factor in the survival of a particular species. The birds are, however, a significant factor in the economy and culture of the people of the Mackenzie Delta region and much of coastal Alaska. This may not always be true, for their social and economic conditions are changing rapidly.

With the native birthrate twice the national average and with hunting technology improving yearly, the day will undoubtedly come when marine birds and other wildlife resources are not able to withstand intensified harvest pressures without more regulation and control. An obvious need exists for government conservation agencies to work more closely with the native people of northern regions in conservation education and development of sound harvest regulations.

_Recreational Uses_

No attempt was made in this evaluation to affix dollar values to every marine bird enjoyed by recreationists. Goldstein (1971), in his economic study of wetlands, found it impossible to fix the value of the production and harvest of migratory waterfowl in Minnesota.

The amount of money spent by recreationists in seeking enjoyment from marine birds does not measure the values they derive; it measures only their costs to participate in such ventures. The analogy that could be made is that the value of a diamond is equal to the cost of mining it. Nevertheless, expenditure data for services and goods provided by air-taxi and charter boat operators and merchants selling bird guides, binoculars, and other outdoor recreational equipment are useful indicators in establishing the secondary or indirect benefits of recreational activities associated with marine birds.

The normal economic concept of net benefits from marine bird recreation would include only those accruing to individuals who provide goods and services to the recreationists, gross revenues minus the costs (Wollman 1962; Pearse and Bowden 1969). This economic return, however, in no way measures direct benefits of marine bird resources to the recreationists.

Another important consideration in evaluating recreational use of marine birds is to recognize that many of the nonparticipants either value the option of being able to take advantage of them in the future, or simply believe that the availability of such resources benefits society (Stegner 1968). Such benefits are difficult, if not impossible, to quantify yet may be exceedingly important due to the uniqueness of the marine bird resource and because many decisions affecting it may prove irreversible.

Increasing numbers of bird enthusiasts throughout North America are discovering the excitement and pleasures derived from visiting marine bird rookeries. As pointed out by Sowl and Bartonek (1974), and as anyone can attest who has ever had the privilege of watching the antics of tufted puffins _(Lunda cirrhata)_ near their colonies on a day when the sun is obscured and the air buoyant, watching seabirds is fun.

We have found that organizations and businesses in practically every North American coastal State and Province, from Nova Scotia to Florida and Alaska to California, are busy scheduling boat or airplane excursions to marine-bird viewing areas off their shores. The Alaska and Washington State ferry systems have for years been providing passengers opportunity to enjoy seabirds of the North Pacific coast. Audubon chapters in San Diego, Los Angeles, Monterey, Seattle, Anchorage, and other cities sponsor annual excursions to seabird colonies.

In 1975 a charter airline service in Anchorage, Alaska, booked 530 people in 51 tours to fly to the Pribilof Islands in the Bering Sea to view the outstanding seabird and fur seal colonies there. Included in the bookings were three National Audubon Society International Ecology Workshops, the Massachusetts Audubon Society, the National Wildlife Federation, and Canadian Nature Federation. Participants paid from $1,500 to $2,000 for these tour packages to Alaska. At $300 to $380 per person, depending on the length of the excursion, the air charter service grossed about $160,000 from these tours (Reeve Aleutian Airways, personal communication).

Fairweather Outings, a small cruise business based in Sitka, Alaska, takes people on wilderness excursions in the west Chichagof-Glacier Bay area of the southeastern part of the State. The seabird rookeries are one of the principal attractions for the 90 people taking these trips each year. Over one-third of the clientele has been from outside Alaska; thus their dollars are new dollars to the State's economy. Fairweather Outings grossed about $11,000 in 1974 (Charles Johnstone, personal communication).

These examples illustrate how seabirds, both directly and indirectly, help small coastal businessmen earn a living. It is also important to recognize that the multiplier effects generated by the expenditures in all of the above examples ripple through the regional and State economies.

Despite the great social and economic significance of such activities along our coasts, apparently no attempt is being made to determine the number of people involved in such pursuits and how much they are spending. A study of the phenomenon would undoubtedly produce startling results.

The Wildlife Management Institute (1975) revealed that the national estimated value of manufacturers' shipments in 1972 was $157 million for camping equipment, $5 million for binoculars, and $19.9 million for bird feed. Sales of wild bird feed have been increasing 5 to 10% per year recently. These are all economic indicators of recreation trends of which enjoyment of marine birds is a part.

A major use of photographic equipment and related products and services is in the natural and scenic areas of the nation. Manufacturers' shipments of photographic equipment, and photofinishing, were valued at $2.3 billion in 1972. A 5% excise tax on these items would have generated nearly $118 million (Wildlife Management Institute 1975).

Since inadequate funding plagues most nongame management initiatives, the Wildlife Management Institute (1975) recommended that Congress authorize a matching grant-in-aid program to benefit nongame fish and wildlife. Funds would be obtained from new manufacturers' excise taxes on designated outdoor recreational equipment to initially yield at least $40 million annually.

The Executive Committee of the International Association of Game, Fish and Conservation Commissioners and the Council of the Wildlife Society have already endorsed model legislation for a State program for nongame wildlife conservation (Madson and Kozicky 1972). We urge that these proposals be given serious consideration in terms of future funding of marine bird conservation programs in North America.

It is encouraging to note that several States, including Washington, Oregon, and California, have recently initiated nongame wildlife programs that have resulted in substantial benefits to their citizens. The California legislature, for example, enacted a law in 1974 to provide a means for individuals and organizations to donate funds for supporting nongame species management. The California Department of Fish and Game has increased its nongame staff and appointed a citizen Nongame Advisory Committee to help develop and implement nongame programs.

Because most species of marine birds are not hunted by sportsmen in North America, this increased emphasis on nongame species may eventually benefit research and management programs for seabirds substantially.

_Scientific Research_

Even now, marine-bird research studies and inventories require the expenditure of several million dollars annually along our coasts. In Alaska a multimillion dollar Federal effort has been initiated to assess the environmental risks of developing offshore petroleum potential in the Gulf of Alaska and five other key areas of the State. These areas represent 60% of the nation's total continental shelf and support some of the largest marine-bird populations in the world. The program to examine life-forms and the physical environment of the petroleum lease areas will require 4 to 5 years to complete. Approximately $1.5 million has been allocated to conduct an environmental assessment of marine bird resources in the first 18 months alone.

The U.S. Fish and Wildlife Service is spending about $40,000 to determine the seasonal occurrence, density, and distribution of marine birds in coastal waters adjacent to new national wildlife refuges in Alaska being proposed pursuant to the Alaska Native Claims Settlement Act of 1971, and almost $200,000 to study and manage migratory birds--including marine birds--on existing refuges.

Although generated by external events (including requirements pursuant to the National Environmental Policy Act of 1969) rather than by the resources themselves, these expenditures at least indirectly reflect a social concern for the welfare of marine birds.

_Citizen Involvement (Social Indicator)_

Another encouraging aspect of seabird conservation and its meaning to society is the increasing involvement of citizens in the issue. Although agencies have not been as responsive as many would like, administration of government at all levels has been shaken and stimulated by citizen participation. As Russell W. Peterson, Chairman of the Council on Environmental Quality, has stated, "Citizen action is the essence of democracy. Citizen movements should be encouraged and expanded. The involvement of people is necessary to counterbalance the disproportionate influence of the professional lobbyists and public relations operators hired to further the special interests of their clients." Mr. Peterson further emphasized that government thrives much better on citizen concern and attention than on indifference and neglect.

Therefore, it is highly significant that the Pacific Seabird Group has many nonprofessional, as well as professional, members and that the 1975 International Symposium on Conservation of Marine Birds of Northern North America had strong citizen involvement and

## participation. As everyone recognizes, nothing works in government

unless people, be they doctors, lawyers, college professors, students, environmentalists, or Indian chiefs, make it work.

Educators must upgrade training in environmental sciences so that an environmental awareness (conservation ethic) is instilled in young people. In this regard, an Alaskan bird study program proposed for Alaska schools by J. G. King, Jr., of the U.S. Fish and Wildlife Service in 1962 deserves close scrutiny. This highly innovative and practical environmental education proposal apparently arrived before its time, for nothing was ever done to institute it. Possibly, now would be a good time to give it a closer look.

Conclusions

Success in more adequately recognizing and using social and economic indicators to strengthen and broaden seabird programs will depend on the ability of the resource management agencies to blend the old with the new. It is obvious to most that new alignments, programs, authorities, and sources of funds are needed, but by themselves, they will not be enough to overcome the continuing massive losses of wildlife habitat due to population growth and technological impacts resulting from various developmental programs.

No marine bird programs will be successful without a strong political base. If this is to be assured, resource agencies must be more responsive to the needs of both consumptive and nonconsumptive users and involve them in their programs from early in the planning process. Because marine birds and the natural environments they inhabit are jointly valued over time and are jointly owned, it is important to ask not only what is efficient from the point of view of the present generation but also what is equitable across generations.

References

Belopol'skii, L. O. 1961. Ecology of sea colony birds of the Barents Sea. (Transl. from Russian.) Israel Program for Scientific Translations, Jerusalem. 346 pp.

Bourne, W. R. P. 1972. Threats to seabirds. Int. Counc. Bird Preserv. Bull. II:200-218.

Brandt, H. 1943. Alaskan bird trails: adventures of an expedition by dogsled to the delta of the Yukon River at Hooper Bay. Bird Research Foundation, Cleveland, Ohio. 464 pp.

Ekblaw, W. E. 1928. The material response of the polar Eskimo to their far arctic environment. Ann. Assoc. Am. Geog. 17(4):147-195.

Goldstein, J. H. 1971. Competition for wetlands in the Midwest: an economic analysis. Resources for the Future, Inc., Washington, D.C. 105 pp.

Jarvis, M. J. F. 1971. Interactions between man and the South African gannet. Biol. Conserv. 3(4):269-273.

Johnson, L. L. 1971. The migration, harvest and importance of waterfowl at Barrow, Alaska. M.S. Thesis. Univ. of Alaska, Fairbanks. 87 pp.

Kessel, B., and D. Saario. 1966. Human ecological investigations at Kivalena. Pages 969-1039 _in_ N. J. Wilimovsky and J. N. Wolfe, eds. Environment of the Cape Thompson region, Alaska. U.S.A.E.C., Div. Tech. Inf., Oak Ridge, Tennessee.

Klein, D. R. 1966. Waterfowl in the economy of the Eskimos on the Yukon-Kuskokwim Delta, Alaska. Arctic 19(4):319-335.

Lockley, R. M. 1973. Man and seabirds. Pages 74-90 _in_ R. M. Lockley. Ocean wanders: the migratory seabirds of the world. Stackpole Books, Harrisburg, Pennsylvania.

Madson, J., and E. Kozicky. 1972. A law for wildlife: model legislation for a State nongame wildlife conservation program. Winchester-Western Division, Conservation Department, East Alton, Illinois. 20 pp.

Pearse, P. H., and G. K. Bowden. 1969. Economic evaluation of recreational resources: problems and prospects. Trans. N. Am. Wildl. Nat. Resour. Conf. 34:283-293.

Pederson, S. 1971. Status and trends of subsistence resource use at Point Hope. Pages 37-89 _in_ B. MacLean, ed. Point Hope project report. Univ. of Alaska, Fairbanks.

Salomonsen, F. 1970. Birds useful to man in Greenland. Pages 169-175 _in_ Productivity and conservation in northern circumpolar lands. International Union for Conservation of Nature and Natural Resources, Morges, Switzerland.

Sanger, G. A. 1972. Preliminary standing stock and biomass estimates of seabirds on the subarctic Pacific region. Pages 589-611 _in_ A. Y. Yakenouti et al., eds. Biological oceanography of the North Pacific. Idemitsy Shoten, Tokyo.

Serventy, D. L. 1958. Mutton-birding. Pages 233-234 _in_ A. H. Chisholm, ed. The Australian Encyclopedia, Vol. 6. Angus and Robertson, Sydney.

Serventy, D. L. 1969. Mutton-birding. Pages 53-60 _in_ K. Taylor, ed. Bass Strait Australia's last frontier. Australian Broadcasting Company, Sydney.

Serventy, D. L., U. Serventy, and J. Warham. 1971. Seabird conservation problems in Australia. Pages 40-44 _in_ D. L. Serventy, U. Serventy, and J. Warham. The handbook of Australian birds. A. H. and A. W. Reed, Sydney.

Sowl, L. W., and J. C. Bartonek. 1974. Seabirds: Alaska's most neglected resource. Trans. N. Am. Wildl. Nat. Resour. Conf. 39:117-126.

Stegner, W. 1968. The meaning of wilderness in American civilization. Pages 192-197 _in_ R. Nash, ed. The American environment: readings in the history of conservation. Addison-Wesley Publishing Co., Reading, Massachusetts.

Tuck, L. M. 1960. The murres. Ottawa, Can. Wildl. Ser. 1. 260 pp.

Wildlife Management Institute. 1975. Current investments, projected needs, and potential new sources of income for nongame fish and wildlife programs in the United States. Wildlife Management Institute, Washington, D.C. 55 pp.

Williamson, K. 1945. The economic importance of seafowl in the Faeroes Islands. Ibis 87:249-269.

Wollman, N., chairman. 1962. The value of water in alternative uses, with special application to water use in the San Juan and Rio Grande basins of New Mexico. Univ. of New Mexico Press, Albuquerque. 426 pp.

FOOTNOTES:

[51] Present address: National Audubon Society, 2 Marine Way, Juneau, Alaska 99801.

Resource Development Along Coasts and on the Ocean Floor: Potential Conflicts with Marine Bird Conservation

by

Donald E. McKnight

Alaska Department of Fish and Game Subport Building Juneau, Alaska 99801

and

C. Eugene Knoder

National Audubon Society Lakewood, Colorado

Abstract

Although development of hard mineral resources, expansion of the timber industry, and resultant increases in human pressures along the North Pacific and Arctic coasts will ultimately adversely affect northern marine bird populations, current and proposed

## activities of the petroleum industry are the

most immediate threat to marine birds. The Federal Government's recently announced plans for oil and gas leasing on the Pacific outer continental shelf eclipse the significance of North Slope and Cook Inlet oil developments. Within a few years, onshore storage facilities and supertankers plying these waters will undoubtedly result in widespread chronic and localized catastrophic contamination of northern marine ecosystems.

Coastal and offshore waters south of the reaches of the seasonal ice pack are tremendously productive, supporting a diverse wealth of bird life throughout the year. Because these ecosystems are relatively stable and the impact of temporal oscillations on the physical environment is not as great as in the Arctic, birds in these areas are probably least susceptible to man's influence on a long-term basis.

Avifaunal associations of the Arctic are less diverse and have shorter food chains than more southerly ones; consequently they are more susceptible to environmental perturbations. Slow growth and maturation rates of arctic species and resultant prolonged population recovery periods further aggravate this situation.

Available knowledge of northern seabirds and their environmental requirements is in inverse relation to the latitude at which they are found and to the ecological stability of the ecosystems involved. Arctic bird associations and their fragile environments are least understood, but are doubtless the most vulnerable to the detrimental effects of man-caused environmental degradation. The paucity of knowledge about them limits the possibility of predicting the consequences of petrochemical exploitation and thereby safeguarding against potential problems. Existing technology and support system capabilities of the oil industry are more poorly defined for arctic areas, further compounding this problem. Regardless of information amassed in the future and precautionary measures taken during exploitation of arctic petroleum reserves, the potential for disastrous and perhaps irrecoverable losses to northern marine bird species and populations is great. Losses of major magnitude could appreciably alter the productivity of northern marine ecosystems.

Although the coastal waters of the northwestern United States and western Canada support a plenitude of marine life, including marine birds, relatively little is known about these ecosystems. Sustained interest in quantitative aspects of this area's marine bird populations has developed only within the past few years. As Sowl and Bartonek (1974) indicated, seabirds are the most visible component of a marine ecosystem and, at the same time, they are the least understood. Management information has been haphazardly gathered, and because seabirds occur in incredibly large numbers in north Pacific and arctic waters, it has been convenient to assume that, in the absence of problems, systematized data gathering and analysis were unnecessary.

The sudden emergence in the late 1960's of Alaska and portions of northwest Canada as potential major oil production areas has changed this situation dramatically. Ongoing and planned petroleum development in the North and the concurrent expansion of hard mineral extraction and logging activities now threaten to adversely affect these marine bird resources. Alaska's human population, which numbered only slightly over 400,000 in 1975, will probably double within the present decade. Doubtless, increased numbers of people, oriented toward mineral and other resource exploitation rather than toward traditional wildland values, will compound these problems. Pressures on State and local governments for increased services necessitated by increasing populations will require additional expenditures. In Alaska, at least, these demands are being imposed before revenues from minerals become available. This necessitates additional oil leases, timber sales, and other means for obtaining immediate funding, thereby adding to the acceleration and irreversibility of industrial expansion into the North.

This atmosphere of change has spawned major government-and industry-supported programs to broaden knowledge of northern marine ecosystems, including their avifauna. There has been a recent flurry of publications on seabird populations and biology and a proliferation of papers stressing the need to learn more about the biota of this area. Nevertheless, environmental impact statements on proposed developmental programs in the North still raise more questions than are being answered. Attempts are being made to apply available information on oil spills, human disturbance, and other aspects of environmental degradation gathered from experiences in other areas to expected problems in northern environments, but one must realize that much of the information gained from experience elsewhere is not applicable to these areas. It is realistic to assume that, until development-related problems occur in the North, biologists cannot estimate the magnitude or ecological dimensions of their effects. However, existing knowledge of ecological "laws" and of the biology of some species provides the base for limited predictive efforts.

It is the purpose of this paper to describe significant current and proposed resource development along the coasts and the ocean floors, to summarize existing knowledge of the ecology of marine birds in these areas, and to identify potential conflicts with marine bird conservation. We hope that identification of these problems will provide impetus to data gathering and management programs necessary for conservation of these valuable resources.

The Region and its Avifauna

The region discussed here encompasses nearly half of the United States and Canadian coastlines, extending from Washington to the eastern edge of the Northwest Territories. Alaska alone has two-thirds of the United States' continental shelf (Bartonek et al. 1971). This region's marine and estuarine waters are some of the most productive in the world and support a diverse wealth of bird life throughout the year. Sanger (1972), for example, estimated total summer standing stocks of some 21 million birds in an area approximating the outer continental shelf from the Bering Strait south along the coasts of the Aleutian Islands and North America to central California. Sanger and King (this volume), to whom more data were available, revised this estimate upward to 45 million. Bartonek et al. (1974) provided estimates of year-round standing stocks of 27 million birds in the Bering Sea alone.

North and east of the Bering Strait, population estimates of the bird fauna are less complete. Swartz (1966) estimated, however, that seabird populations of five colonies in the vicinity of Cape Thompson in the Chukchi Sea exceeded a total of 420,000 breeding birds in 1960. Information provided by Bartonek and Sealy (this volume) indicates that large colony complexes at Cape Lisburne and Little Diomede Island each number, in aggregate, over 1 million breeding birds, mainly alcids, kittiwakes (_Rissa_ spp.), gulls (_Larus_ spp.), fulmars _(Fulmarus glacialis)_, and cormorants (_Phalacrocorax_ spp.). Although the Chukchi Sea coast north of Cape Lisburne has no rocks suitable for cliff-nesting seabirds, large numbers of tundra-nesting species use the inshore waters as a migratory pathway, and many nonbreeding cliff nesters summer in these waters (J. M. Scott, comments by Pacific Seabird Group on U.S. Department of the Interior Draft Environmental Statement 74-90). According to Scott, sea ducks and gulls are the most numerous birds in the Beaufort Sea. Observations by Thompson and Person (1963) of an estimated 1 million eiders, mostly king eiders _(Somateria spectabilis)_ and Pacific eiders _(S. mollissima)_, passing over Point Barrow en route to molting areas, reflect the numbers involved. Oldsquaws _(Clangula hyemalis)_ use coastal waters of the Beaufort Sea for postbreeding wing molts; Bartels (1973) estimated their numbers at nearly 400,000 in the fall and perhaps more during the molting period. Shorebirds, jaegers (_Stercorarius_ spp.), gulls, and terns, most of which use coastal waters at some time during the summer season, swell bird numbers by several millions in this area (Arctic Institute of North America 1974).

As indicated by Sanger (1972), the seabirds inhabiting coastal areas south of Bering Strait are mainly members of the Procellariidae in summer and Alcidae in winter. Sooty shearwaters _(Puffinus griseus)_ are the prevalent summer species and ancient murrelets _(Synthliboramphus antiquus)_ and marbled murrelets _(Brachyramphus marmoratus)_ are the most abundant winter species. Sanger's central subarctic domain (offshore waters including the Gulf of Alaska) had a different species composition. During the summer, procellariids--mostly slender-billed shearwaters _(Puffinus tenuirostris)_ and sooty shearwaters--made up 94% of the biomass. Procellariids, including fulmars, larids (largely glaucous-winged gulls, _Larus glaucescens_), black-legged kittiwakes _(Rissa tridactyla)_, and large alcids, including the tufted puffin _(Lunda cirrhata)_, made up 87% of the winter biomass in this domain (Sanger 1972).

Although most of the arctic waters, including the Bering, Chukchi, and Beaufort seas, are unavailable to birds during the winter because of pack ice, they seasonally host an avifauna dominated by colony nesters, such as common and thick-billed murres (_Uria aalge_ and _U. lomvia_), and tundra nesters, such as oldsquaws and eiders. In far northern waters, sea ducks (mainly eiders and oldsquaws), red phalaropes _(Phalaropus fulicarius)_, and gulls are the predominant species.

Intertidal areas throughout the Alaska, British Columbia, and Washington coasts support characteristic assemblages of shorebirds, including the black oystercatcher _(Haematopus bachmani)_, rock sandpiper _(Erolia ptilocnemis)_, wandering tattler _(Heteroscelus incanum)_, surfbird _(Aphriza virgata)_, and black turnstone _(Arenaria melanocephala)_ as reported by J. M. Scott (comments by Pacific Seabird Group to U.S. Department of the Interior Draft Environmental Statement 74-90). Perhaps the greatest concentrations of shorebirds in this whole region occur during spring and fall migrations in Prince William Sound. The tremendous numbers of migrating birds using these tidal and marsh areas are hard to imagine, but densities of up to 250,000 shorebirds per 259 hectares (ha) on portions of the more than 51,820-ha tidal flats of the Copper River Delta have been recorded (Isleib and Kessel 1973).

Although this region's avifauna is remarkable from the numerical standpoint, it is important to remember also that some of its species are limited in distribution to this area. According to Bartonek et al. (1971), Alaska is the only known breeding area for black turnstones, bristle-thighed curlews _(Numenius tahitiensis)_, surfbirds, western sandpipers _(Ereunetes mauri)_, and Kittlitz's murrelets _(Brachyramphus brevirostris)_. Several waterfowl species, including the dusky Canada goose _(Branta canadensis occidentalis)_, cackling Canada goose _(B. c. minima)_, Aleutian Canada goose _(B. c. leucopareia)_, and Aleutian common teal _(Anas crecca nimia)_ nest only in Alaska coastal areas (Bartonek et al. 1971). Izembek Lagoon on the Alaska Peninsula annually hosts the entire population of black brant, _Branta nigricans_ (Hansen and Nelson 1957), and many other waterfowl, seabird, and shorebird species nest or live in this region in numbers important to their worldwide welfare.

Current and Planned Resource Development

The immense nonrenewable resource wealth of Alaska and other arctic regions has remained virtually unrecognized or unexploited until recently because of the availability of these resources in more accessible locations. As supplies have diminished or been exhausted elsewhere and demands have increased, however, it has become economically feasible or necessary to tap supplies in less-accessible regions. For this reason, the petroleum industry has recently expanded its exploratory efforts in the far North with well-known success. Deposits of metallic ores, coal, and other raw materials to feed industry have likewise been discovered and plans devised for their extraction and sale. Pressed with decreased availability of commercial timber elsewhere, the logging industry has similarly begun to broaden its efforts into Alaska. Expansion of industrial activities into the North is proceeding at a rapidly accelerating pace, and these industries, their associated support industries, and expanded human populations are having and will continue to have unprecedented impact on these marine ecosystems, including their avifauna.

_Petroleum Development_

The existence of potentially marketable oil and gas deposits in Alaska has been recognized since the early 1900's, but it was not until the Swanson River, Alaska, oil field was discovered in 1957 and later developed that the Arctic entered the modern era of oil development (McKnight and Hiliker 1970). This field and offshore fields in the Upper Cook Inlet basin have been producing oil for nearly a decade. The discovery of petroleum reserves on Alaska's North Slope and Canada's Mackenzie River Delta is common knowledge, and a pipeline has been constructed to transport Alaska oil to a tanker facility at Valdez in Prince William Sound. Alternative proposals to pipe North Slope natural gas along the existing corridor to a facility in Prince William Sound or to build a new pipeline to take this gas to existing fields, and a planned pipeline on the Mackenzie River Delta and south through Canada, are being considered. Construction of a gas liquefaction facility in Prince William Sound and tanker traffic through the Sound and the Gulf of Alaska are potential ramifications of an Alaska gas pipeline.

As McKnight and Hiliker (1970) and Bartonek et al. (1971) pointed out, the greatest potential problem for marine bird populations from North Slope oil will be associated with the operations of the Alyeska Pipeline system's terminal at Valdez. Oil storage and ship-loading facilities at this port and heavy tanker traffic through Prince William Sound represent a pollution source that could result in significant seabird and waterfowl mortalities. Certainly, development of gas liquefaction facilities in the Sound, with inherent increases in human populations and tanker traffic, would compound this potential problem.

Although future impacts from existing petrochemical developments are cause for concern, the Federal Government's recently announced plans for oil and gas leasing on the Pacific outer continental shelf (Fig. I) eclipse the significance of North Slope and Cook Inlet oil developments. It now appears the Gulf of Alaska is the most favorable area of the outer continental shelf for oil and gas production (Council on Environmental Quality 1974). This area, covering more than 10.3 million ha, has already been subjected to extensive seismic investigations, and estimates of its undiscovered, economically recoverable crude oil and natural gas resources range from 3 to 25 billion barrels and 15 to 30 trillion cubic feet, respectively (Council on Environmental Quality 1974).

[Illustration: Fig. 1. North Pacific, showing portions of the outer continental shelf being considered for gas and oil leasing by the Federal Government (vertical hatching) and areas leased or proposed for leasing by the State of Alaska (cross hatching).]

Kinney et al. (1970) reported that in Cook Inlet, Alaska, an estimated 0.3% of the oil produced and handled in offshore platform wells is spilled. Several routine offshore operations result in discharges of oil and other materials into water, and, unlike accidental spills, the probability of their occurrence is 100% (Council on Environmental Quality 1974). During drilling operations, cleaned drilling mud and drill cuttings are discharged overboard. Drilling mud may consist of such substances as bentonite clay, caustic soda, organic polymer, proprietary defoamer, and ferrochrome lignosulfate. Waters from geological formations are often produced and discharged into the sea while the wells are in production. These waters may be fresh or saline, and often contain small amounts of oil. All of these pollutants increase the adverse effects of offshore oil production, and when potential spills are also considered, the ultimate impact on the marine ecosystem may be substantial.

The State of Alaska has already leased offshore sites in Kachemak Bay, and present considerations for future leases in the lower Cook Inlet and Beaufort Sea further reflect the widespread and massive nature of petrochemical developments in the Arctic planned for the next 2 decades (Fig. 1). Proved crude oil reserves are less than 1 billion barrels and natural gas reserves are less than 2 trillion cubic feet in Cook Inlet, but it appears that undiscovered recoverable oil and gas resources may be much greater (Council on Environmental Quality 1974). There are also indications that known onshore oil reserves along Alaska's northwest coast will soon be opened for development by the Arctic Slope Regional Corporation, landowners in the area as a result of the Native Land Claims Act of 1971. This group is at least considering the transportation of these petroleum products to market in tankers, from an open-water port in the Chukchi Sea--thereby adding to the tanker traffic in northern waters.

_Hard Mineral Resource Development_

As indicated by Bartonek et al. (1971), there has been renewed interest in opening up Alaska's hard mineral resources to economic development as new transportation routes and modes have been developed. Plans are being completed to develop the Bering River coal field, with the eventual goal of exporting coking coal to Japan. Although mining operations might ultimately affect freshwater environments to the detriment of several waterfowl species, including the trumpeter swan _(Olor buccinator)_, the chief cause for concern will be additional freighter traffic through Prince William Sound. Similar plans to develop Klukwan and Snettisham iron deposits in southeastern Alaska for the use of Japanese industry (Bartonek et al. 1971) may result in the imposition of further traffic in Alaska shipping lanes.

Plans are under way to strip-mine coal deposits in the Beluga field near the west side of Cook Inlet and transport a coal slurry via pipeline to a thermal electric generation plant opposite Anchorage on the Inlet. Impact on tidal areas may be minor, but thermal pollution of the waters is a possibility.

Development plans for tin and tungsten deposits in the Lost River area of Alaska's Seward Peninsula are under way after several years of faltering starts and stops. These activities and possible extraction of gold lying offshore from Nome may ultimately have some effect on these coastal areas. Methods for recovering gold, regardless of the type, would disrupt marine and estuarine environments used by marine birds (Bartonek et al. 1971), and transportation of ores would also increase freighter traffic in the Bering Sea.

_Timber Resource Development_

Although the timber industry has long been established along the coast from Washington north through southeastern Alaska, timber harvests are rapidly expanding on U.S. Forest Service lands in Alaska. The impact of this industry is principally on terrestrial ecosystems, but certainly log rafting in estuarine areas, disposal of wastes from pulp mills, and freighter traffic transporting wood pulp or logs to Japan and west coast markets contribute to the chronic degradation of marine bird environments. Recent meager studies on the Vancouver Canada goose _(Branta canadensis fulva)_ in southeastern Alaska have pointed out the importance to this species of coastal timber stands for nesting and estuarine environments for brood rearing and wintering. This essentially nonmigratory goose (Hansen 1962) may be particularly vulnerable to logging activities in these areas. Similarly, recent evidence indicates that marbled murrelets may nest in large conifer trees adjacent to the coast, from northwestern California to northern southeastern Alaska (Harris 1971; Savile 1972). If this is true, logging may eventually greatly restrict the breeding of this numerically important inhabitant of northern coastal waters.

Assessment of Resource Development and Potential Conflicts with Marine Bird Conservation

Although extraction of hard mineral resources, expansion of the timber industry, and resultant increases in human pressures along North Pacific and Arctic coasts will ultimately affect northern marine bird populations, current and proposed activities of the petroleum industry pose the most immediate threat to marine birds. Chronic degradation of estuarine and marine coastal waters by logging wastes, pulp mill and sewage effluents, and bilge oils is an insidious process, the impacts of which will be difficult, at best, to quantify. Results of a major oil spill or even low-level contamination of marine ecosystems with oil will be more apparent, however. For this reason, and the fact that the industry is expanding rapidly into the North, most of this discussion will be directed at the impacts of oil development on northern marine birds.

Potential sources of adverse environmental degradation affecting these birds resulting from oil and gas exploration, development, and production include: (1) oil discharges into marine waters, both chronic and catastrophic, (2) gravel excavation and dumping in coastal areas, (3) seismic activities, (4) discharge of drilling mud and drill cuttings into marine waters, including toxic heavy metal constituents of drilling mud, (5) disturbance resulting from petrochemical

## activities, and (6) increased human populations resulting in

interference with critical life processes and increased hunting of game species. Each source of environmental change will vary by latitudinal and seasonal factors in their effects upon the birds. We consider herein only coastal and ocean floor developments and their anticipated generalized impacts on populations.

Although this is a discussion of "northern" marine birds, it is important to remember that we are considering a diverse avifauna existing in an environmental gradient from temperate to polar regions. In general, the more southerly portions of this marine environment are characterized by a greater diversity of species, more complex food chains, and a resultant greater stability (Dunbar 1968). Arctic marine ecosystems, on the other hand, are characterized by numerical dominance by a few species, relatively simple food chains, and an inherent instability or fragility (Dunbar 1968). According to Dunbar, arctic systems are regulated primarily by temporal oscillations in the physical environment, whereas biological interactions (e.g., competition, predation) are considered more significant in the maintenance of temperate and tropical ecosystems.

Because of their relative instability, arctic ecosystems are more susceptible to alteration by extreme environmental perturbation, either natural or man-imposed (Burns and Morrow 1973). Slow growth and maturation rates of the avian constituents of these ecosystems and resultant long recovery periods (Ashmole 1971) further aggravate this situation.

Regardless of their seasonal availability, these arctic waters constitute some of the most productive areas for seabirds in the western hemisphere (Bartonek et al. 1974). Upwelling, nutrient-rich waters, combined with intense and prolonged incident radiation, result in lush phytoplankton "blooms" that form the foundation of relatively simple but numerically strong plant and animal communities (Ashmole 1971). A relatively small number of avian species have evolved to take advantage of this seasonally available food supply, and the ability to migrate to lower latitudes in winter is a characteristic of most arctic-nesting species. Because summers are short in arctic regions, early arrival and a synchronous breeding schedule are necessary to enable the young to leave the breeding grounds before severe weather conditions prevail (Ashmole 1971). Arrival of these birds generally coincides closely with the earliest availability of nesting habitat and food (Williamson et al. 1966). Migration, molting, and reproduction place tremendous stresses on these birds, and as a result, arctic-nesting species tend to reproduce less often and at older ages than do those of more temperate regions (Ashmole 1971).

In spite of these adaptations, arctic bird species tread a thin line between extinction and survival, and natural disasters take a heavy toll. Bailey and Davenport (1972) reported a massive mortality in a pelagic population of common murres in Bristol Bay, Alaska, during April 1970. They felt that this disaster, resulting in the death of probably 100,000 or more birds, most likely resulted from starvation precipitated by severe weather. Barry (1968) reported a similar loss to starvation of about 100,000 eiders along the Beaufort Sea coast during the extremely cold spring of 1964. Observers along Alaska's Beaufort Sea reported finding eiders and oldsquaws dead and dying from the effects of cold weather in 1970 (Bartonek et al. 1971). It is readily apparent that the tenuous existence into which these birds have evolved leaves them particularly vulnerable to the man-induced stress of developments during the arctic summer.

_Direct Effects of Oil Pollution_

The most obvious, and perhaps the most disastrous consequence of petrochemical development on northern marine bird populations is that of a major oil spill or a well blowout into marine waters. Although temperate and tropical waters are apparently able to assimilate oil spills and chronic pollution from petroleum and its products (Nelson-Smith 1972), this has not been demonstrated to be true for arctic waters. In fact, studies in the Beaufort Sea have shown that the bacteria that degrade oil do not use hydrocarbons at the ambient temperatures of the Arctic (Glaeser and Vance 1971). Therefore, a large oil spill in the Arctic could persist for many years. As demonstrated by Campbell and Martin (1973), the diffusion and transport mechanisms generated by the pack-ice dynamics of the Beaufort Sea and the slow rate of oil biodegradation under arctic conditions would combine to diffuse an oil spill over the sea and eventually deposit oil on the ice surface. This, in turn, would lower the natural albedo over a large area and melt the ice in the area of the spill. This pack ice supports an under-ice community which is an important food source for phalaropes, jaegers, gulls, terns, and other seabirds (Watson and Divoky 1972).

As indicated by Nelson-Smith (1972) many investigators have stated that a spot of oil "no bigger than a dollar" on the breast of a bird is enough to bring about death by exposure, at least in the colder seas. It is easy to see the relative vulnerability of already stressed birds in arctic areas to a spill, and because of the concentration of these birds in available open-water areas, possibilities for catastrophic mortalities are evident.

Such disasters already have occurred in north Pacific waters. Dickason (1970) reported an incident in which diesel oil reaching the Alaska coast, probably from the sinking of two Japanese freighters some distance offshore, affected an estimated 90,000 murres. J. G. King, Jr. (cited in Bartonek et al. 1971) estimated that at least 100,000 birds, mostly alcids and waterfowl, died in the vicinity of Kodiak Island during winter 1970 as a result of oil pollution (probably ballast dumped by tankers entering Cook Inlet). It must not be forgotten that chronic pollution in similar areas where oil development and transport

## activities are taking place probably kills more birds every year than

die after a single catastrophic spill. Total annual losses due to oil in the North Sea and North Atlantic, excluding disasters, amount to 150,000 to 450,000 seabirds (Nelson-Smith 1972).

That oil pollution, both chronic and catastrophic, can dramatically affect populations of marine birds has already been demonstrated elsewhere. Uspenskii (1964) reported that more than 30,000 wintering oldsquaws perished from oil pollution near Botland Island in the Baltic and that in later years this species had almost disappeared from Swedish Lapland. Jackass penguins _(Spheniscus demersus)_, found only in South Africa, have suffered losses from pollution caused by oil traffic around the Cape of Good Hope (Stander and Venter 1968). Their total population was estimated at 100,000 in 1960, and in two separate but not isolated incidents 1 to 2% of this number were known to have been killed by oil. Unknown but considerable numbers were uncounted or were lost at sea. Colony nesters, including puffins _(Fratercula arctica)_, razorbills _(Alca torda)_, and murres in the southerly portions of the North Sea are declining rapidly (Nelson-Smith 1972). Puffins, which numbered 100,000 on Annet in the Scilly Isles in 1907, were reduced to 100 birds by 1967; by then, colonies farther east on the Great Britain coast were already extinct. Pollution from the _Torrey Canyon_ disaster alone killed five-sixths of the puffins in the main French colony on the Sept Isles in Brittany and reduced the razorbills to a mere 50 birds, one-ninth of previous numbers (Bourne 1970).

There is every reason to believe that similar reductions in numbers could occur along the tanker route from Valdez to Puget Sound, with localized extirpation of colonies. Even more disastrous, however, would be an inopportune well blowout or other major spill in arctic waters. Massed concentrations of birds, already stressed by severe weather and food shortages, would be extremely vulnerable to this type of situation.

As pointed out by Nelson-Smith (1972), peculiarities of bird behavior determine, to some extent, the vulnerability of a species to oil spills. Auks, murrelets, and puffins (all Alcidae), loons (_Gavia_ spp.), grebes (_Podiceps_ spp.), and diving ducks may be most susceptible to oiling. Auks and loons, because they float low in the water, may more readily become completely covered by oil. Diving species that become flightless during their molt, such as alcids and waterfowl, or which do not fly because of social bonds between adults and flightless young (common murre) and spend most of their lives on the water, would be particularly vulnerable (J. M. Scott, comments by Pacific Seabird Group on U.S. Department of the Interior Draft Environmental Statement 74-90). All divers can easily surface into oil, and their reaction is to dive again, which in a large spill could result in surfacing into more oil. Phalaropes (_Phalaropus_ spp.), which flock to feed in eddies which concentrate drift, may similarly be vulnerable to adverse effects of oil that would also concentrate in these areas. On the other hand, gulls swimming along the surface are likely to take wing before becoming seriously contaminated.

Nelson-Smith (1972) reported that gannets _(Morus bassana)_, which collected oiled sea-weed for building nest mounds, contaminated themselves and their eggs. Behavioral problems associated with oil spills can be more subtle, however, and Darling's (1938) conclusions that the display of adjacent males contributes to stimulation of the female during courtship in seabirds breeding in massed colonies, is a good example. If Darling was correct, this behavioral characteristic could further impede the recovery of a population of auks, for example, from mortalities resulting from catastrophic losses to spills.

* * * * *

On the basis of this information it is possible to predict that alcids, which make up the bulk of the birds inhabiting the coastal areas during winter (Sanger 1972), would be very susceptible to oil spills from future tanker traffic in these waters. The potential exists, therefore, for a tremendous impact (from a single inopportune oil spill) upon these species and upon the entire ecosystem. Sea ducks too, because of their diving behavior, propensity for flocking, and flightless molt period, would be very vulnerable to oil spills. Wintering flocks of oldsquaws and several species of scoters along the coasts of Alaska, British Columbia, and Washington can be expected to dwindle as North Slope oil begins to be transported to Puget Sound ports.

It is recognized now that seabirds transfer and recycle nutrients and energy between trophic levels and between regions of an ocean (Sowl and Bartonek 1974). Although the significance of this role in the marine ecosystem can only be surmised at present, conservative estimates by Sanger (1972) indicated that birds consume from 0.6 to 1.2 million tons of food and return from 0.12 to 0.24 million tons of feces into the subarctic Pacific region annually. G. A. Sanger's (personal communication) revised estimates of these bird populations indicated that his 1972 estimates should be doubled. Regardless, it appears that the disastrous effects of such a spill would extend beyond the bird populations involved.

_Indirect Effects of Oil Pollution and Petrochemical Developments_

By no means would direct losses attributable to contamination by oil be the only threat to marine bird populations as a result of petrochemical expansions into these waters. Some water birds that become contaminated with nonlethal doses of petroleum during the breeding season are not likely to breed (J. M. Scott, comments by Pacific Seabird Group on U.S. Department of the Interior Draft Environmental Statement 74-90). Viability of embryos is greatly reduced when the eggshell becomes smeared with oil from the contaminated plumage of the female (Hartung 1965). Degradation of habitat, particularly to nesting areas and food supplies, will certainly occur, and its most pronounced effects will be felt in the Arctic. Gravel removal for construction of offshore drilling pads, causeways, and onshore production facilities would displace nesting birds and, combined with subsequent discharge of drill cuttings, perhaps have an adverse impact on bottom food organisms. Nesting habitat loss through destruction or the inability of birds to accept disturbance could be substantial, particularly along the Beaufort Sea coasts of Alaska and Canada, where offshore barrier islands and tundra-covered islands provide protection from mammalian predators for nesting by Pacific eiders, Sabine's gulls _(Xemia sabini)_, Arctic terns _(Sterna paradisaea)_, black guillemots _(Cepphus grylle)_, and other species (Arctic Institute of North America 1974). Flaxman Island near the mouth of the Canning River is a tundra island supporting a nesting population of whistling swans _(Olor columbianus)_, and the only nesting colony of the Alaska snow goose _(Chen caerulescens)_ is on Howe Island in the Sagavanirktok River Delta (Arctic Institute of North America 1974).

* * * * *

Although there would probably be little actual nesting habitat loss for cliff-nesting species, human disturbance to colonies during the nesting period, particularly from helicopter and fixed-wing aircraft flybys, could have considerable impact (Sowl and Bartonek 1974). The "living waterfall" effect of thousands of seabirds pouring off a rookery is truly spectacular, but each such occurrence during incubation and brooding periods causes a rain of eggs or young to fall from the cliffs (Sowl and Bartonek 1974). Temporarily abandoned chicks and eggs are susceptible to predation by gulls or jaegers.

Even for species nesting on level ground, aircraft overflights close to breeding colonies may cause major losses to young and eggs. Sladen and LeResche (1970) reported that flights by an LH-34 helicopter (at 305 m altitude) over an Adelie penguin _(Pygoscelis adeliae)_ colony caused some egg loss. Landing this aircraft 183 m from the colony caused 50 to 80% of the birds to flee territories, resulting in egg and chick loss. Disturbance caused by visitors walking through or near nesting areas of the South African gannet _(Sula capensis)_ on Bird Island, Lamberts Bay, South Africa, caused desertion of nesting sites (Jarvis and Cram 1971). Studies of disturbance on breeding black brant, Pacific eiders, glaucous gulls _(Larus hyperboreus)_, and arctic terns at Nunaluk Spit and Phillips Bay, Yukon, in July 1972 indicated that human presence was the most critical form of disturbance affecting incubating behavior of these species (LGL Limited 1972_a_). Disturbance by aircraft--especially helicopters--affected the normal incubating behavior of all species except Pacific eiders. Nesting success of black brant and arctic terns was reduced by this disturbance.

Disturbance can adversely affect molting birds. The process of molting places heavy energy demands on birds, and particularly on waterfowl whose molt results in a flightless period; few areas provide adequate protection from predators necessary during this period. Prime molting areas are scarce along the arctic coast, yet are vital to the welfare of thousands of sea ducks and seabirds. Studies conducted by LGL Limited (1972_b_) indicated that aircraft traffic over sea duck molting areas altered normal behavior, and therefore had a detrimental effect. Recommendations resulting from these studies were that air traffic be suspended over these areas during the molting season.

For some arctic-nesting waterfowl, premigration staging activity, during which fat reserves to sustain southward migration are stored, is a very important component of the annual cycle (Delacour 1964). Snow geese, breeding mainly in arctic Canada, concentrate in large numbers on staging grounds along the Beaufort Sea coast of eastern Alaska and the Yukon. Because gas compressor stations would be required along the proposed arctic gas pipeline route, experimental studies were conducted in September 1972 to determine the effect of disturbance from sounds generated by compressors (LGL Limited 1972_c_). These studies indicated that compressor noise was disruptive to staging geese.

Indirect effects on marine bird resources resulting from development

## activities may ultimately prove to be more detrimental than the

aforementioned direct factors. It is conceivable that the impact of these industries, mainly on the benthic and demersal fauna of the coastal areas, could greatly lower the carrying capacity of this habitat for marine birds (Bartonek et al. 1974). Because of the simplified and short arctic food chains and the lack of alternative food sources in these areas, arctic ecosystems would be particularly vulnerable to this type of problem (Burns and Morrow 1973).

Ecological or toxic influences on several food species could result in substantial declines in bird populations. In the Arctic, where temperatures are low, and bacterial and other decompositional

## activities are consequently slow, spilled oil would persist for many

years, with concomitant deleterious effects on the marine organisms of the area (Burns and Morrow 1973). Reduced recruitment of young would no longer balance inevitable or density-independent population mortality (Ashmole 1971). Although indications are that arctic species are the most vulnerable to this type of impact, the lack of knowledge of the feeding niches of most seabirds discourages further evaluation of this potential problem. It is obvious, however, that ecology of arctic birds is least understood, and these species are the most vulnerable to the detrimental effects of man-caused environmental degradation.

Conclusions

Predictability of the impact of resource development on marine birds in northern waters is limited by our relative ignorance of these birds and their ecology. Just as there exists a latitudinal gradient in the ecological stability of the ecosystems involved, available knowledge of these ecosystems is in inverse relationship to the latitude at which they occur. Arctic bird associations and their fragile environments are least understood but are doubtless the most vulnerable to the detrimental effects of man-caused environmental degradation. Existing technology and support system capabilities of the oil industry are poorly defined for Arctic areas, further compounding this problem (Arctic Institute of North America 1974).

Although activities associated with the extraction of hard minerals and the timber industry will ultimately affect northern seabirds, petrochemical developments pose the most immediate threat to this resource. Exploration and development of many coastal and offshore sedimentary basins with a potential for oil or gas production are proceeding rapidly. Within a few years, oil storage and loading facilities at Valdez, Alaska, and supertankers plying northern waters will probably result in widespread chronic and localized catastrophic contamination of northern marine environments. Experience in other areas has demonstrated that oil spills are a considerable potential threat to these bird populations, directly through widespread mortality and indirectly through effects on the environment. This threat is of such magnitude that entire populations or species could be lost to a single spill if it occurred at the wrong place at the wrong time of year. Because many of these species require 3 to 4 years for maturation and may rear only one or two young per year, recovery time for their populations is great (Ashmole 1971). For these and other reasons, the Council on Environmental Quality (1974) concluded that the Gulf of Alaska appeared more vulnerable to major environmental damage from outer continental shelf oil and gas development than sites off the Atlantic coast.

As Bartonek et al. (1971) pointed out, it would be a national tragedy if the great nongame bird populations along Alaska's coast were decimated during the "Environmental Decade" without even being properly described. Regardless of information amassed in the future and precautionary measures taken during exploitation of arctic petroleum reserves, the potential for disastrous and perhaps irrecoverable losses to northern marine bird species and populations is great. Losses of major magnitude could appreciably alter the productivity of northern marine ecosystems, to the detriment of other renewable resources.

Knowledge of northern marine birds, their environments, and their ecology must be greatly expanded if the consequences of petrochemical exploitation are to be predicted and safeguards established against potential problems. To the extent possible, oil exploration and development activities should be limited to temperate, more stable, marine ecosystems, at least until more northerly areas are better understood. Similarly, these activities must be conducted in such places and at such times that impact on the environment will be minimized. State and federal governments and the petroleum industry are ultimately answerable for this responsibility.

The Nation must be aware of the potential costs of energy independence set forth as a goal of proposed oil and gas leasing of Alaska's outer continental shelf. We must ask ourselves if we are willing to risk extermination of species to reach this goal, or if we can afford the luxury of reducing the biological productivity of these waters.

References

Arctic Institute of North America. 1974. The Alaskan arctic coast--a background study of available knowledge. 551 pp.

Ashmole, N. P. 1971. Seabird ecology and the marine environment. Pages 223-286 _in_ D. S. Farner and J. R. King, eds. Avian biology. Vol. I. Academic Press, New York.

Bailey, E. P., and G. H. Davenport. 1972. Die-off of common murres on the Alaska Peninsula and Unimak Island. Condor 74(2):215-219.

Barry, T. W. 1968. Observations on natural mortality and native use of eider ducks along the Beaufort Sea coast. Can. Field-Nat. 82(2):140-144.

Bartels, F. B. 1973. Bird survey techniques on Alaska's north coast. M.S. Thesis. Iowa State Univ., Ames. 47 pp.

Bartonek, J. C., J. G. King, and H. K. Nelson. 1971. Problems confronting migratory birds in Alaska. Trans. N. Am. Wildl. Nat. Resour. Conf. 36:345-361.

Bartonek, J. C., R. Elsner, and F. H. Fay. 1974. Mammals and birds. Pages 23-28 _in_ E. J. Kelley and D. W. Hood, eds. Probes: a prospectus on processes and resources of the Bering Sea shelf, 1975-1985. Univ. Alaska, Inst. Mar. Sci. Publ. Inf. Bull. 74-1.

Bourne, W. R. P. 1970. Special review after the "Torrey Canyon" disaster. Ibis 112:120-125.

Burns, J. J., and J. E. Morrow. 1973. The Alaskan Arctic marine mammals and fisheries. Arctic oil and gas problems and possibilities, 5th International Congress. 24 pp.

Campbell, W. J., and S. Martin. 1973. Oil and ice in the Arctic Ocean: possible large-scale interactions. Science 181:56-58.

Council on Environmental Quality. 1974. OCS oil and gas--an environmental assessment. Vol. I. Washington, D.C. 214 pp.

Darling, F. F. 1938. Bird flocks and the breeding cycle; a contribution to the study of avian sociability. Cambridge Univ. Press, N.Y.

Delacour, J. 1964. The waterfowl of the world. Vol. IV. Country Life Ltd., London. 364 pp.

Dickason, O. E. 1970. Center for short-lived phenomena event report. Smithsonian Institution, Cambridge, Massachusetts, 36(1970):926.

Dunbar, M. J. 1968. Ecological development in polar regions. A study in evolution. Prentice-Hall, Inc., Englewood Cliffs, N.J. 119 pp.

Glaeser, J. L., and G. P. Vance. 1971. A study of the behavior of oil spills in the Arctic. U.S. Coast Guard, Office of Research and Development, Washington, D.C. 60 pp.

Hansen, H. A. 1962. Canada geese of coastal Alaska. Trans. N. Am. Wildl. Nat. Resour. Conf. 27:301-320.

Hansen, H. A., and U. C. Nelson. 1957. Brant of the Bering Sea--migration and mortality. Trans. N. Am. Wildl. Nat. Resour. Conf. 22:237-256.

Harris, R. D. 1971. Further evidence of tree nesting in the marbled murrelet. Can. Field-Nat. 85(1):67-68.

Hartung, R. 1965. Some effects of oiling on reproduction of ducks. J. Wildl. Manage. 29(4):872-874.

Isleib, M. E., and B. Kessel. 1973. Birds of the north gulf coast--Prince William Sound region, Alaska. Biol. Pap. Univ. Alaska 14. 149 pp.

Jarvis, M. J. F., and D. L. Cram. 1971. Bird Island, Lamberts Bay, South Africa: an attempt at conservation. Biol. Conserv. 3(4):269-272.

Kinney, P. J., D. K. Button, D. M. Schell, B. R. Robertson, and J. Groves. 1970. Quantitative assessment of oil pollution problems in Alaska's Cook Inlet. Univ. Alaska Inst. Mar. Sci. Rep. R-69-16. 43 pp.

LGL Limited. 1972_a_. Disturbance studies of breeding black brant, common eiders, glaucous gulls and Arctic terns at Nunaluk Spit and Phillips Bay, Yukon Territory. Report prepared for Northern Engineering Service, Ltd. 50 pp.

LGL Limited. 1972_b_. Aircraft disturbance to molting sea ducks, Herschel Island, Yukon Territory. Report prepared for Northern Engineering Service, Ltd. 31 pp.

LGL Limited. 1972_c_. Gas compressor noise simulator disturbance to snow geese, Kamakuk Beach, Yukon Territory. Report prepared for Northern Engineering Service, Ltd.

McKnight, D. E., and B. L. Hiliker. 1970. The impact of oil development on waterfowl populations in Alaska. Proc. Western Assoc. State Game Fish Comm. 50:286-297.

Nelson-Smith, A. 1972. Oil pollution and marine ecology. Paul Elek, Ltd., London. 260 pp.

Sanger, G. A. 1972. Preliminary standing stock and biomass estimates of seabirds on the subarctic Pacific region. Pages 589-611 _in_ A. Y. Takenouti et al., eds. Biological oceanography of the North Pacific. Idemitsu Shoten, Tokyo.

Savile, D. B. O. 1972. Evidence of tree nesting by the marbled murrelet in the Queen Charlotte Islands. Can. Field-Nat. 86(4):389-390.

Sladen, W. J. L., and R. E. LeResche. 1970. New and developing techniques in antarctic ornithology. Pages 585-616 _in_ M. W. Holdgate, ed. Antarctic Ecology. Vol. I. Academic Press.

Sowl, L. W., and J. C. Bartonek. 1974. Seabirds--Alaska's most neglected resource. Trans. N. Am. Wildl. Nat. Resour. Conf. 39:117-126.

Stander, G. H., and J. A. V. Venter. 1968. Oil pollution in South Africa. Pages 251-259 _in_ Proceedings of the International Conference on Oil Pollution of the Sea.

Swartz, L. G. 1966. Sea-cliff birds. Pages 611-678 _in_ N. J. Wilimovsky and J. N. Wolfe, eds. Environment of the Cape Thompson region, Alaska. U.S.A.E.C., Div. Tech. Inf., Oak Ridge, Tennessee.

Thompson, D. Q., and R. A. Person. 1963. The eider pass at Point Barrow, Alaska. J. Wildl. Manage. 27(3):348-356.

Uspenskii, S. M. 1964. Present day problems of nature conservation in the Arctic. Problems of the North 7:171-178.

Watson, G. E., and G. J. Divoky. 1972. Pelagic bird and mammal observations in the eastern Chukchi Sea, early fall 1970. Pages 111-172 _in_ C. I. Merton et al., eds. An ecological survey in the eastern Chukchi Sea. U.S. Coast Guard Oceanogr. Rep. 50.

Williamson, F. S. L., M. C. Thompson, and J. Q. Hines. 1966. Pages 437-480 _in_ N. J. Wilimovsky and J. N. Wolfe, eds. Environment of the Cape Thompson region, Alaska. U.S.A.E.C., Div. Tech. Inf., Oak Ridge, Tennessee.

Mortality to Marine Birds Through Commercial Fishing

by

Warren B. King

International Council for Bird Preservation Smithsonian Institution, Washington, D.C.

R. G. B. Brown

Canadian Wildlife Service Dartmouth, Nova Scotia, Canada

and

Gerald A. Sanger[52]

U.S. National Marine Fisheries Service Seattle, Washington

Abstract

Commercial fishing has been responsible for incidental mortality of seabirds for centuries, but with the advent of offshore salmon gill-net fishing in the North Pacific in 1952 and in the North Atlantic in 1965, the magnitude of this kill has increased, and there is strong indication that populations of some seabirds are being adversely affected. Murres (_Uria_ spp.) are most frequently killed, although several other species are caught in lesser numbers. The seabird resources of several nations are involved in this mortality. Longline fishing and inshore gill-net fishing for salmon and cod also are responsible for mortality of seabirds, although usually not in significant numbers.

That the activities of commercial fishermen have caused mortality of marine birds surprises no one nowadays. Traditions of exploitation of marine birds by fishermen date from previous centuries, and fishing has contributed to the extinction of some species. For example, great auks _(Pinguinus impennis)_ and other birds were used as food by fishermen fishing for Atlantic cod _(Gadus morhua)_ on the Grand Banks of Newfoundland since the beginning of that fishery in the early 16th century (Collins 1884; Lucas 1890). The last great auk died in 1844, but smaller species, such as storm-petrels (Hydrobatidae), greater shearwaters _(Puffinus gravis)_, and black-legged kittiwakes _(Rissa tridactyla)_, were used for food until rather recently (Templeman 1945). This practice has now lapsed, however.

Inshore Fisheries

Until the advent of the offshore salmon gill-net fisheries in the North Pacific in 1952 and the North Atlantic in 1965, most seabird mortality in these areas was the result of local fishing close to shore. Several records of such bird mortality have been published. For example, 8,000-10,000 seabirds--presumably mostly alcids--were reported caught annually off Hammerfest in northern Norway (Holgersen 1961). E. Brun (personal communication) reported that the longline fishery off the coast of Norway is having serious consequences on Norwegian populations of murres.

Numbers of alcids are caught in nets set for Atlantic salmon _(Salmo salar)_ around the coasts of Ireland and Scotland (Biddy 1971). A similar situation exists along the west Greenland coast, although it is overshadowed there by the direct exploitation of huge numbers of alcids by hunting. Nonetheless, in 1967 for example, 15,000 alcids were recovered from fish nets in southwestern Greenland, where they were sold as food (Evans and Waterston 1976). The annual salmon catch of the west Greenland inshore fishery has fluctuated between 60 and 1,500 metric tons and has averaged about 1,000 tons. There are no data comparing the relative catch of birds and fish in this fishery.

Atlantic cod follow the spawning capelin _(Mallotus villosus)_ inshore along the east coast of Newfoundland in late June and early July. They are traditionally fished with traps and handlines along this coast, but there has been a recent trend toward using drift nets set on the bottom. Since alcids feed extensively on capelin at this time, many are caught in the cod nets set in areas close to the large colonies off Witless Bay (D. N. Nettleship, personal communication). Additionally, gill nets are set at the surface for salmon in the same area. Common murres _(Uria aalge)_ are most affected, but Atlantic puffins _(Fratercula arctica)_ are also taken.

There are as yet no estimates of the total alcid mortality from this fishery, although the annual catch of birds is believed to be smaller during the present than during the last decade because the fishing effort is reduced, and fishermen in the area now avoid setting nets near alcid concentrations because of the annoyance of having to remove the birds from their nets. The Witless Bay colonies contain over 77,000 pairs of common murres, or 11% of the total eastern North American population, and over 235,000 pairs of Atlantic puffins, or 71% of the North American population outside of Greenland (Brown et al. 1975). The potential danger is obvious.

There are few data on mortality of seabirds from inshore commercial fisheries in the North Pacific. Some mortality of alcids has been shown to take place in Cook Inlet, Alaska, from beach-netting for Pacific salmon (_Oncorhynchus_ spp.) adjacent to seabird rookeries and from drift-netting in the inlet (D. A. Snarski, personal communication), but this mortality has not been quantified.

Bilateral agreements between the United States and Japan, the U.S.S.R. and the Republic of Korea, concerning the use of inshore waters adjacent to some of the Aleutian Islands, Kodiak, Nunivak, St. Matthew, St. George, Kayak, and Forrester Islands permit trawling, longlining, and loading fish and fuel in some of these areas and at certain periods. Although these activities may affect the seabirds of these areas, the extent of the effects are not known (U.S. Department of the Interior, Alaska Planning Group 1974). Murie (1959) indicated, however, that the disappearance of the ancient murrelet _(Synthliboramphus antiquus)_ from Sanak Island, Gulf of Alaska, was probably due as much to fisheries as to the blue fox industry. It has been suggested that the Japanese murrelet _(Synthliboramphus wumizusumi)_ may have declined as the result of fishing activities near breeding sites off the coast of Japan (Bourne 1971).

Atlantic Offshore Gill-net Fishery

In 1965, Denmark began an offshore gill-net fishery for Atlantic salmon in the Davis Strait off the coast of west Greenland. The offshore fishery catch increased from 36 metric tons in 1965 to more than 1,200 metric tons in 1969, and then gradually decreased.

The fact that large numbers of seabirds--almost entirely thick-billed murres _(Uria lomvia)_--were being drowned in the salmon gill nets was brought to the attention of the International Council for Bird Preservation at its 15th World Conference in 1970. The Council's recommendation was submitted to the Danish government and stated: "... having noted that during the 1969 fishing season about 250,000 individuals of Brunnich's guillemot or thick-billed murre _(Uria lomvia)_, a pelagic diving bird, were caught in these drift nets and drowned, which number represents no less than 25 percent of the Greenland population and exceeds its annual reproductive capacity; urges the Danish Government, and the national governments of all other countries involved in this fishing, to take all possible measures to eliminate this very serious problem."

The figures in the recommendation were not supported by research; they appeared instead to have been derived from the observed mortality on an offshore fishery vessel in 1965, which was then related to the salmon catch on that vessel and applied to the total catch of the inshore fishery in 1964 (Anonymous 1969). Studies in 1969 and 1970 by the Fisheries Research Board of Canada finally gave a firm basis for the earlier, though poorly substantiated concern. On the basis of the assumption that the ratio of salmon to murres caught in experimental fishing applied to the commercial fishery, an estimate of an annual mortality of 0.5 million murres (±50%) was made on the basis of a salmon catch of 1,200 metric tons (Tull et al. 1972).

The birds being killed were from colonies in west Greenland, the eastern Canadian Arctic, and possibly east Greenland and Spitzbergen. Coupled with other known causes of mortality (particularly hunting on the Greenland and Newfoundland coasts, an unknown but definitely substantial kill from oil pollution, a calculated mortality of pre-fledging young, and an unknown natural post-fledging mortality) there is no doubt that the estimated annual production of 1.5 million chicks from west Greenland and the Canadian Arctic was less than the estimated total annual mortality (Tull et al. 1972). Thus, it comes as no surprise that recent surveys of murre populations of west Greenland and the Canadian Arctic have revealed massive declines in numbers (Evans and Waterston 1976; D. N. Nettleship, personal communication). It is therefore encouraging news that, as a result of an agreement between the United States and Denmark, the offshore salmon gill-net fishery was terminated at the end of the 1975 season. The inshore fishery remained in operation, however, but was restricted to a total annual salmon catch of 1,100 metric tons.

Pacific Offshore Salmon Gill-net Fishery

In the north Pacific Ocean, the Japanese gill-net fisheries for salmon (_Oncorhynchus_ spp.), which have operated since 1952, might be expected to have an even more destructive effect on seabirds, since the annual salmon catch by the three Japanese salmon drift-net fisheries was about one hundred times that in west Greenland in recent years. The first, the mothership fishery, comprising about 369 catcher-boats[53] serviced by 11 mother-ships, operates west of 175°W and generally north of 46°N during the summer. The second, the land-based fishery of about 325 ocean-going vessels, operates west of 175°W and south of 46°N; and the third, the coastal fishery, made up of about 1,380 short-haul vessels, operates off Hokkaido. The relative salmon catches of these three fisheries is on the order of 1:1.34:0.65.

Data collected on U.S. National Marine Fisheries Service research vessels in 1974 (obtained through the cooperation of Francis M. Fukuhara and Richard Bakkala, Northwest Fisheries Center, Seattle, Washington) give, for the first time, an estimate of the magnitude of the incidental seabird kill of the Japanese salmon gill-net fishery. The kill data are available only from the mothership area and from an area east of it to 165°W. The Japanese salmon fishery is restricted to waters west of 175°W by agreement with the United States. Bird kills from the other two areas may be estimated by the relative salmon catch figures for the areas, assuming that seabird densities, species composition, and catch effort are similar.

An estimate of the total kill of seabirds in the mothership area may be made by calculating the bird mortality per length of gill-net set by research vessels, multiplied by the total length of gill nets set by the 369 catcher-boats of the Japanese mothership fishery. About 4,666 km of nets are set and retrieved daily during the approximately 65-day fishing season. The estimated annual mortality in the mothership area is about 75,000 to 250,000 birds. The lower number is based on data from 10 cruises (450 km of nets set) west of 175°W, within the area of the mothership fishery. The higher number is based on data from 20 cruises, including those in the first figure, west of 165°W, and covering the period 18 April to 3 September 1974 (956 km of nets set), whereas the mothership fishery usually operates between mid-May and late July. Assuming similar seabird densities and catch per unit of effort in the areas of the land-based and coastal fisheries, the estimated annual mortality is between 214,500 and 715,000 birds. Since 1952, as many as 4.7 million birds may have been killed by the Japanese salmon gill-net fishery. It must be stressed that seabird densities and catch per unit of effort are not known to be similar for the areas in question; consequently the projection of bird kill figures from one area to all three is speculative.

In the mothership area and adjacent seas to the east, in addition to murres (48% of birds killed), significant numbers of shearwaters, _Puffinus_ spp. (27%); puffins (9%); and fulmars, _Fulmarus glacialis_ (5%) are killed, as are lesser numbers of small alcids, albatrosses (_Diomedea_ spp.), and storm-petrels. The murres and puffins taken in the mothership area are of U.S. and U.S.S.R. origin, and the shearwaters come from New Zealand, Australia, and Chile. In the coastal fishery area, Japanese and U.S.S.R. alcids are taken. Available knowledge of the populations of the species making up the bulk of the kill, which has been taking place for 20 years, is insufficient to suggest whether their annual reproduction can tolerate such losses. Prohibition of fishing within 160 km of North Pacific seabird breeding islands would help to decrease losses of alcids of U.S. origin, but would not help the shearwaters from the southern hemisphere.

Comparison of statistics of the salmon fisheries and associated bird kills from the North Atlantic and the North Pacific shows that the North Atlantic salmon fishery is concentrated in a relatively small area which is also along a major migration pathway of murres. Virtually all seabird mortality is confined to one species. Enough information is at hand to indicate that this cause of mortality, in conjunction with others known to be significant, is causing a drastic decline in the thick-billed murre population.

In the North Pacific, on the other hand, the fishery is more widely dispersed and the ratio of seabirds to salmon caught is much lower. Furthermore, several species are subject to mortality. No information is available to indicate whether alcid populations (which make up two-thirds of the kill) are stable or decreasing. The shearwaters, primarily sooty _(Puffinus griseus)_ and slender-billed _(P. tenuirostris)_, appear to be able to sustain not only these losses but also a sizable harvest of birds of the year (the so-called muttonbirds) on their New Zealand and Australian breeding grounds. Thus, although the latest estimates of the total standing stock of seabirds in the North Pacific in summer may be as high as 100 million (Sanger and King, this volume), and thus only about 1 of every 200 birds in the North Pacific region may be caught, the fact that a few species, particularly murres, are selectively caught raises questions about the impact of this fishery on populations of these species.

The U.S.-Japan Migratory Bird Convention of 1973 specifically protects all of the species thought to be subject to gill-net mortality in the Pacific. Thus, the Japanese salmon fleet apparently operates in constant violation of this convention.

Mortality of Albatrosses

A recent analysis of recoveries of Laysan albatrosses _(Diomedea immutabilis)_ and black-footed albatrosses _(D. nigripes)_ banded on the northwest Hawaiian chain from 1937 to 1969 showed that of a sample of 532 recovered birds, 57.4% of the Laysan species and 49.5% of the black-footed species were caught on fishhooks or in nets, and the means of recovery of many additional birds was thought to have been the same (Robbins and Rice 1974). It is likely that the large majority are taken on Japanese and U.S.S.R. longline tuna fishing gear. Although this cause of mortality is insignificant in terms of the total population of either species (only 0.2% of banded Laysan and 0.8% of banded black-footed albatrosses have been recovered by any means away from their breeding grounds), these species are protected by the U.S.-Japan Migratory Bird Convention. Furthermore, the possibility exists that individuals of the endangered short-tailed albatross _(Diomedea albatrus)_ might be killed in this manner.

Long-term Effects of Developing Capelin Fishery in Northwest Atlantic

Capelin are important food fish for many seabirds in the northwest Atlantic, and the development and expansion of this fishery off eastern Canada must be carefully monitored. In theory, the capelin fishery ought not to seriously affect the birds because it is designed to exploit a surplus of capelin artificially created by the overfishing of Atlantic cod, the capelin's most important predator. It is hoped that there is no prospect of the overfishing that may have contributed to the recent drastic decline of the Peruvian anchovy _(Engraulis ringens)_ and the seabird species dependent on it (Paulik 1971). However, the relative influence of overfishing and "El Niño" oceanographic conditions on the decline remains unclear. North Atlantic seabirds are, in any case, more versatile in their feeding habits (Belopol'skii 1961). But, the threat may be a subtle one. The important point to the seabirds may well be not merely the survival of a reasonably large capelin stock, but the presence of capelin schools in high densities in certain areas or at certain seasons. Lower densities might, for example, reduce the foraging efficiency of breeding birds, and hence their nesting success. The very large common murre colony on Funk Island, Newfoundland (500,000 pairs: Tuck 1960), might be

## particularly vulnerable. It lies close to an area where capelin are

especially abundant and one which is already being exploited by the developing fishery.

References

Anonymous. 1969. Seabird slaughter. Sports Fish. Inst. Bull. 203:5.

Belopol'skii, L. O. 1961. Ecology of sea colony birds of the Barents Sea. (Transl. from Russian.) Israel Program for Scientific Translations, Jerusalem. 346 pp.

Biddy, C. J. 1971. Auks drowned by fishnets. Seabird Rep. No. 2.

Bourne, W. R. P. 1971. General threats to seabirds. ICBP [Int. Counc. Bird Preservation] Bull. 11:200-219.

Brown, R. G. B., D. N. Nettleship, P. Germain, C. E. Tull, and T. Davis. 1975. Atlas of eastern Canadian seabirds. Canadian Wildlife Service, Ottawa. 220 pp.

Collins, J. W. 1884. Notes on the habits and methods of capture of various species of seabirds that occur on the fishing banks off the east coast of North America and which are used as bait for catching codfish by New England fishermen. U.S. Comm. Fish Fish. Rep. 1882:311-335.

Evans, P., and G. Waterston. 1976. The decline of the thick-billed murre in Greenland. Polar Rec. 18:283-286.

Holgersen, H. 1961. On the movements of Norwegian _Uria aalge_. (In Norwegian, English summary.) Sterna 4:229-240.

Lucas, F. A. 1890. Expedition to the Funk Island, with observations on the history and anatomy of the Great Auk. Rep. U.S. Natl. Mus., 1887-1888:493-529.

Murie, O. J. 1959. Fauna of the Aleutian Islands and Alaska Peninsula. U.S. Fish Wildl. Serv., N. Am. Fauna 61. 406 pp.

Paulik, A. J. 1971. Anchovies, birds, and fishermen in the Peru Current. Pages 156-185 _in_ W. W. Murdoch, ed. Environmental Resources and Society. Sinauer Associates, Inc., Stamford, Conn.

Robbins, C. S., and D. W. Rice. 1974. Recoveries of banded Laysan albatrosses _(Diomedea immutabilis)_ and black-footed albatrosses _(D. nigripes)_. Pages 232-271 _in_ W. B. King, ed. Pelagic studies of seabirds in the Central and Eastern Pacific Ocean. Smithson. Contrib. Zool. 158.

Templeman, W. 1945. Observations on some Newfoundland seabirds. Can. Field-Nat. 59:136-147.

Tuck, L. M. 1960. The murres. Canadian Wildlife Service, Ottawa. 260 pp.

Tull, C. E., P. Germain, and A. W. May. 1972. Mortality of thick-billed murres in the west Greenland salmon fishery. Nature (Lond.) 237 (5349):42-44.

U.S. Department of the Interior, Alaska Planning Group. 1974. Final environmental impact statement, proposed Alaska Coastal National Wildlife Refuges. 678 pp.

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._

---------------------------------------------- Catch Species (metric tons) ---------------------------------------------- Fish Pollock 1,500,000 Flatfish 125,000 Pacific cod 45,000 Herring 35,033 Salmon 11,785 Sablefish 7,000 Pacific halibut 222 Other 40,000 Shellfish King crabs 26,798 Snow crabs 17,694 Shrimp Minor ----------------------------------------------

[Illustration: =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.]

[Illustration: =Fig. 2.= Areas of major winter and spring concentrations of Pacific herring in Bristol Bay and the Bering Sea.]

[Illustration: =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:

_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

[Illustration: 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.

Table 2. _Fish of worldwide commercial importance in the diets of some marine birds._

-------------------------------------------------------- Fish Shearwaters 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.

[Illustration: 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.)

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Yusa 1954 (cm)[54] Tanino et al. 1959 =Walleye pollock= 31-35 95,700 Feb.- April Kobayashi 1963 (_Theragra_ 46-50 324,400 June -May Musienko 1963, 1970 _chalcogramma_ Serobaba 1968 Pallas) Hart 1973[55]

Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.1-0.2 0-10 Feb.-June { 12 at 6-7°C { 20.5 at 3.4°C[57] Larval 0.4-0.9 10-25 March-? > 25 at 6-7°C Larval 0.9-? 25-? ?-Sept. ? Juvenile 2.2-4.1 0-?[58] Summer -- Juvenile 6.0-30.0 4-37 Summer -- Adult 30.0-70.0 0-386 -- --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Moiseev 1953 (cm)[54] Mukhacheva and =Pacific cod= 60 1,200,000 Jan.- ? Zviagina 1960 (_Gadus_ 78 3,300,000 March Musienko 1970; _macrocephalus_ Hart 1973[55] Tilesius)

Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.1-0.11 100-250 Demersal { 8-9 at 11°C { 17 at 5°C { 28 at 2°C Larval 0.5-3.2 25-150 Feb.-Aug. ? Juvenile ? 10-? Summer -- Adult 40.0-99.0 0-900 -- --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Stevenson 1962 (cm)[54] Musienko 1970 =Pacific herring= 20.5-22.0 26,600 May- Varies Rumyantsev and (_Clupea_ 28.0-31.0 77,800 June Darda 1970 _harengus pallasi_ Reid 1972 Valenciennes) Hart 1973[55]

Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.1-0.2 0-12 Demersal 10-20[57] Larval 0.9 0.5-8 May-June } Larval 1.3 0.5-8 June-July } 42-56 Larval 2.5 1-6 July-Aug. } Juvenile 2.5-20.5 0-? March-Nov. -- Adult 20.5-31.0 0-140 March-Nov. --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period (cm)[54] Clemens and =Capelin= ? 3,000 June- ? Wilby 1961 (_Mallotus_ ? 6,000 July Musienko 1970 _villosus_ 10.3 6,670 Hart 1973 (Muller)) ? 60,000 Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.1 <20 Demersal 14-? Larval 0.5-? ? June-? ? Juvenile ? ? March-Nov.(est.) -- Adult ? 0-? March-Nov. --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Musienko 1963, 1970 (cm)[54] Kashkina 1970 =Pacific sand lance= -- ? June- [59] Hart 1973 (_Ammodytes_ Aug. _hexapterus_ Pallas) Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg ? ? Demersal ? Larval 0.7-3.4 0-? June-Sept. ? Juvenile 3.6-9.6 0-? ? -- Adult 26 0-? ? --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Paraketsov 1963 (cm)[54] Lisovenko 1965 =Pacific ocean perch= 26 10,000 March- ? Lyubimova 1965 (_Sebastes_ 44 180,000 May Kashkina 1970[60] _alutus_ (Gilbert))

Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg[61] -- -- -- -- Larval[62] 0.6-? [62] March-Aug. ? Juvenile 6.2 37-128 -- -- Juvenile 10.4 37-154 -- -- Juvenile 14.7-21.3 37-230 -- -- Adult 21.3-51.0 37-420 -- --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period (cm)[54] Novikov 1964 =Pacific halibut= 75 101,723 Oct.- ? Hart 1973 (_Hippoglossus_ 135 2,800,837 March _stenolepis_ Schmidt) Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.3-0.4 40-935 Oct.-March 48 at ? Larval 0.8-1.5 >200 Nov.-May } Larval 1.5-2.9 <100 May-Sept.} 70-98 Juvenile 3.4-4.2 7-43 -- -- Juvenile 19-25 7-45 -- --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Moiseev 1953 (cm)[54] Pertseva-Ostraumova =Yellowfin sole= 1954; Musienko 1963; (_Limanda_ 26.1-28.0 1,295,000 June- July Fadeev 1965; _aspera_ 40.1-42.0 3,319,500 Aug. Kashkina 1965_a_, (Pallas)) 1965_b_[55] Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 0.07-0.09 >0 June-Aug. 9.4 at 13.1°C[57] Larval 0.2-1.2 >0 July-Oct. ? Juvenile 2.1-2.5 5-15 -- --

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period (cm)[54] Kurata 1960, 1964 =King crabs= 9.4 55,408 April- ? Korolev 1964 (_Paralithodes_ 17.1 444,651 June Rodin 1970 _camtschatica_ (Tilesius))

Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days) Egg -- 100-200[63] -- ? Zoeal} 0.55-0.65 ? April-July {33 at 7-10°C Zoeal} {23 at 12.3-12.5°C Glaucothoeal 0.38x0.18 ? May-? ? Juvenile ? 1-? -- ?

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Haynes 1973[55] (cm)[54] Jewett and =Snow crabs= Haight[64] (_Chionoecetes_ ? ? ?[65] ? _bairdi_ Rathbun) Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg 100[63] -- ? Prezoeal 0.22-0.28 ? May-? 1-2 at 2.5°C 1st zoeal 0.50-0.56 ? Summer ? 2d zoeal ? 0-10 Summer ? Megalopal 0.30-0.35x ? Summer -- 0.18-0.21 Juvenile 0.44-0.48x ? -- -- 0.32-0.35

Fecundity Spawning season Source of data Length Mean no. Total Peak of female of eggs period period Ito 1968; Kon 1970 (cm)[54] Haynes 1973; =Snow crabs= Motoh 1973 (_Chionoecetes_ ? ? ?[65] ? Jewett and _opilio_ Haight[64] (O. Fabricius)) Total Depth from Seasonal Duration of Life length surface period of life stages stage (cm)[56] (m) pelagic life (days)

Egg ? 93[60] -- ? Prezoeal -- ? May-? } 1st zoeal 0.48-0.54 ? Summer } 2d zoeal 0.62-0.71 ? Summer } 63-66 at 11-13°C Megalopal 0.29-0.33 ? Summer } 0.19 Juvenile 4.4-4.8x ? -- -- 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.

[Illustration: 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._

Pacific Food Walleye Pacific ocean Yellowfin Pacific item Herring Salmon pollock cod perch sole halibut

Invertebrates Pteropods X X -- -- X -- -- Squid -- X -- X X -- X Polychaetes X X X X -- X X Copepods X X X -- -- -- -- Amphipods X X X X X X -- Euphausiids X X X -- X X -- Decapods X X X X X X X

Fish Capelin X X X X -- X -- Sand lance -- X X X -- -- X

Table 5. _Forage fish and invertebrate foods eaten by seven species of marine birds in the eastern Bering Sea._

Shear- Food item waters Murres Puffins Murrelets Fulmars Kittiwakes Gulls

Forage fish Sand lance X X X -- -- X X Capelin -- -- X -- -- -- --

Invertebrates Copepods -- -- -- -- -- X -- Euphausiids X X -- -- -- X -- Amphipods X X -- -- -- X -- Decapods X X -- -- -- X -- Pteropods -- X -- -- -- -- -- Chaetognaths -- -- -- -- -- -- -- Polychaetes -- X X -- -- X -- Squid X X -- -- 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).

[Illustration: 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.

[Illustration: 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.

[Illustration: =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.

References

Ahlstrom, E. H. 1959. Vertical distribution of pelagic fish eggs and larvae off California and Baja California. U.S. Fish Wildl. Serv. Fish. Bull. 60(161):107-146.

Ahlstrom, E. H. 1961. Distribution and relative abundance of rockfish (_Sebastodes_ spp.) larvae of California and Baja California. Int. Comm. Northwest. Atl. Fish. Spec. Publ. 3:169-176.

Ashmole, N. P. 1971. Sea bird ecology and the marine environment. Pages 223-286 _in_ D. S. Farner, J. R. King, and K. C. Parkes, eds. Avian Biology. Vol. 1. Academic Press, New York.

Bartonek, J. C., and D. D. Gibson. 1972. Summer distribution of pelagic birds in Bristol Bay, Alaska. Condor 74(4):416-422.

Bourne, W. R. P. 1963. A review of oceanic studies of the biology of seabirds. Proc. Int. Ornithol. Congr. 13:831-854.

Brett, J. R., M. Hollands, and D. F. Alderdice. 1958. The effect or temperature on the cruising speed of young sockeye and coho salmon. J. Fish. Res. Board Can. 15(4):587-605.

Carlson, H. R. 1977. Food habits of juvenile sockeye salmon, _Oncorhynchus nerka_, in the inshore coastal waters of Bristol Bay, Alaska. Fish. Bull. 74(2):458-462.

Chitwood, P. E. 1969. Japanese, Soviet, and South Korean Fisheries off Alaska, development and history through 1966. U.S. Fish Wildl. Serv. Circ. 310. 34 pp.

Clemens, W. A., and G. V. Wilby. 1961. Fishes of the Pacific Coast of Canada. Fish. Res. Board Can., Bull. 68, 2d ed. 443 pp.

Donaldson, L. R., and F. J. Foster. 1941. Experimental study of the effect of various water temperatures on the growth, food utilization, and mortality rates of fingerling sockeye salmon. Trans. Am. Fish. Soc. 70:339-346.

Fadeev, N. S. 1965. Comparative outline of the biology of flatfishes in the southeastern part of the Bering Sea and the condition of their resources.