more specifically the waters between 6 and 60 m deep. The shallow
waters of continental shelves are some of the most productive of
sea waters, but are among the least studied. Although some species
(black-legged kittiwakes, tufted puffins, and fulmars) move into deep
waters, many species of marine birds of northern waters gather in
large numbers on preferred feeding grounds at or near the edges of
continental shelves during their winter season (Fisher 1952; Tuck 1960).
8. To know more about the potential effects of proposed developments on
seabirds and waterfowl.
a. To prepare models which will predict probabilities of contamination
of breeding and feeding areas (summer, winter, and during migration)
using existing knowledge of
(1) areas of proposed mineral development;
(2) areas that will be influenced by secondary development such as
dredging new harbors, laying subsurface pipelines;
(3) tidal and oceanic currents;
(4) numbers of marine birds or waterfowl using specific geographic
areas and habitats (e.g., waters below nesting cliffs, feeding grounds,
wintering grounds, and gatherings during migration);
(5) the distribution and patchiness of habitats (i.e., the redundancy
among and within habitats and the degree to which populations exchange
between alternative habitats);
(6) the biological importance of species in local ecosystems (Are they
predators whose effects increase diversity?);
(7) the human importance of the species (Are they endemics? Do they
have unusual "charisma" for the public?);
(8) the vulnerability of the species (Is its distribution restricted?
Is it subject to oil pollution? Are their preferred grounds near areas
of high development potential?);
(9) the types of biological effects (e.g., oil contamination of
plumage, PCB contamination of food chains); and
(10) whether the potential impacts are reversible or irreversible and
to what degree.
b. To understand more of the effects of hunting on the behavior of
marine birds and waterfowl on their breeding grounds, and to assess the
effects on breeding performance of changes in behavior which result
from human activities (such as hunting or studying the birds).
c. To understand the effects of the presence of predators (whether
introduced or native) on breeding colonies in order to assess the
importance of removing the predators or preventing their access to
breeding grounds.
The Relation of the Products of Biological Research to Programs for
Conservation of Marine Bird Resources
Although peaceful coexistence of wildlife populations and economic
development are here assumed to be practical, some new social
institutions are needed to control damaging activities of people during
economic development. Human activities and industrial products which
damage wildlife or their habitat must be identified, as must the space
and resources which wildlife require for survival and health.
1. What seabird cliffs, islands, lagoons, wetlands, river mouths, and
other habitat features are of first importance for breeding or for
maintaining the populations? Some small areas of habitat are critical
for the survival of some species during periods of stress. Those
habitats need official recognition. Steps are needed to ensure that the
habitats are maintained.
2. What physical expressions of economic development are of little,
modest, or serious impact on wildlife and its habitat? These activities
and constructions include harbors, storage sites, transshipment
facilities, roads, pipelines, summer camps, and suburban or vacation
developments.
3. What kinds of human activities will disturb, damage, or change the
behavior or accessibility of wildlife? Many activities of one group of
people have secondary effects which affect the enjoyment of resources
for other groups. These include
a. gill netting for salmon, which may kill large numbers of murres and
diving ducks;
b. release of predators on seabird nesting islands, which may kill
adults or inhibit their feeding their young;
c. free running of pets (such as dogs and cats) over wetlands or
wildlife habitat, because pets are predators and harass the wildlife
which may be feeding;
d. flights of aircraft, especially helicopters, near or over seabird
cliffs because such flights may cause serious damage to eggs and young;
e. hunting, because the game becomes timid and flees from those who
might enjoy watching wildlife;
f. snow machines, because their presence is disagreeable to many and
they provide easy access by which disturbing activities may reach into
areas where wildlife would otherwise be undisturbed.
4. What limitations or alterations are needed in the existing
legal institutions, such as the Marine Mammals Protection Act, the
instruments implementing native land claims, the process of Alaska
State lands withdrawal, the conditions for leasing State and Federal
lands for development of mineral resources, and traditional rights
of private property? All of these legal institutions are relevant to
problems of wildlife survival and restoration, and within most of
these institutions there exist conflicts between rights and benefits
of special political interests and the husbanding of renewable common
property resources.
Experience in Europe and in New England suggests that if reasonable
limitations are set on human activities and that if adequate money
charge is made against those who profit by economic development to
defray full social costs, wildlife can continue to do well. In most
cases where damage has occurred it is because those who administer the
public institutions have failed to include consideration of the common
property resources.
References
Ainley, D. G., and T. J. Lewis. 1974. The history of Farallon
Island marine bird populations. Condor 76(4):432-446.
Ames, P. L., and G. S. Mersereau. 1964. Some factors in the decline
of the osprey in Connecticut. Auk 81(2):173-185.
Andrewartha, H. G., and L. C. Birch. 1954. The distribution and
abundance of animals. Univ. Chicago Press, Chicago, Ill. 782 pp.
Ashmole, N. P. 1963. The regulation of numbers of tropical oceanic
birds. Ibis 103b:458-473.
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. 1967. Geese of the Anderson River delta, Northwest
Territories. Ph.D. Thesis. Univ. of Alberta, Edmonton, Alberta,
Canada. 176 pp.
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.
Bédard, J. 1969. Feeding of the least, crested, and parakeet
auklets around St. Lawrence Island, Alaska. Can. J. Zool.
47:1025-1050.
Belopol'skii, L. O. 1961. Ecology of sea bird colonies of the
Barents Sea. (Translated from Russian.) Israel Program for
Scientific Translations, Jerusalem. 346 pp.
Bent, A. C. 1919. Life histories of North American diving birds.
U.S. Natl. Mus. Bull. 107. 245 pp.
Bent, A. C. 1921. Life histories of North American gulls and terns.
U.S. Natl. Mus. Bull. 113. 345 pp.
Bent, A. C. 1922. Life histories of North American petrels and
pelicans and their allies. U.S. Natl. Mus. Bull. 121. 343 pp.
Bergman, G. 1957. Concerning the problem of mixed colonies: the
tufted duck and gulls. Die Vogelwarte 19(1):15-25.
Bertram, G. C. L., D. Lack, and B. B. Roberts. 1934. Notes on East
Greenland birds, with a discussion of the periodic non-breeding
among arctic birds. Ibis 13(4):816-831.
Brown, R. G. B. 1967. Breeding success and population growth
in a colony of herring and lesser black-backed gulls _Larus
argentatus_ and _L. fuscus_. Ibis 109(4):502-515.
Buckley, F. G., and P. A. Buckley. 1971. The breeding ecology
of royal terns _(Sterna [thalasseus] maxima maxima)_. Ibis
114(3):344-359.
Buckley, P. A., and F. G. Buckley. 1975. The significance of
dredge spoil islands to colonially nesting waterbirds in certain
national parks. Proc. Conf. on Management of Dredge Islands
in North Carolina Estuaries, May 1974. N.C. Sea Grant Publ.
UNC-SG-75-01, Raleigh.
Byrd, G. V., D. D. Gibson, and D. L. Johnson. 1974. The birds of
Adak, Alaska. Condor 76(3):288-300.
Coulson, J. C. 1966. The influence of the pair-bond and age on the
breeding biology of the kittiwake gull _Rissa tridactyla_. J.
Anim. Ecol. 35:269-279.
Coulson, J. C. 1968. Differences in the quality of birds nesting
in the centre and on the edges of a colony. Nature 217 (Feb.
3):478-479.
Coulson, J. C. 1974. Kittiwakes _Rissa tridactyla_. Pages 134-141
_in_ S. Cramp, W. R. P. Bourne, and D. Saunders, The Seabirds of
Britain and Ireland. Taplinger Publ. Co., Inc., New York. 287 pp.
Coulson, J. C., G. A. Potts, I. R. Deans, and S. M. Fraser. 1968.
Exceptional mortality of shags and other seabirds caused by
paralytic shellfish poison. Brit. Birds 61:381-404.
Coulson, J. C., and E. White. 1958. The effect of age on the
breeding biology of the kittiwake _Rissa tridactyla_. Ibis
100(1):40-51.
Coulson, J. C., and E. White. 1961. An analysis of the factors
influencing the clutch-size of the kittiwake. Proc. Zool. Soc.
Lond. 136:207-217.
Cramp, S., W. R. P. Bourne, and D. Saunders. 1974. The seabirds of
Britain and Ireland. Taplinger Publ. Co., Inc., New York. 287 pp.
Darwin, C. 1859. On the origin of species by means of natural
selection. John Murray, London. 490 pp.
Dement'ev, G. P., R. N. Meklenburtsev, A. M. Sudilovskya, and E. P.
Spangeberg. 1968. Birds of the Soviet Union. Vol. 2. (Translated
from Russian.) Israel Program for Scientific Translations,
Jerusalem. 553 pp.
Drost, R., E. Focke, and G. Freytag. 1961. Entwicklung und aufbau
einer population der Silbermöwe, _Larus argentatus argentatus_.
J. Ornithol. 102(4):404-429.
Drury, W. H. 1961. Observations on some breeding water birds on
Bylot Island. Can. Field-Nat. 75(2):84-101.
Drury, W. H. 1963. Results of a study of herring gull populations
and movements in southeastern New England. Pages 207-217 _in_
Colloque: Le problème des oiseaux sur les aérodromes (Nice,
1963). Inst. Nat. Rech. Agron., Paris.
Drury, W. H. 1973. Population changes in New England seabirds.
Bird-Banding 44(4):267-313.
Drury, W. H. 1974_a_. Population changes in New England seabirds.
Bird-Banding 45(1):1-15.
Drury, W. H. 1974_b_. Rare species. Biol. Conserv. 6(3):162-169.
Drury, W. H., and I. C. T. Nisbet. 1972. The importance of
movements in the biology of herring gulls in New England. Pages
173-212 _in_ Population Ecology of Migratory Birds: a Symposium.
U.S. Fish Wildl. Serv. Wildl. Res. Rep. 2. 278 pp.
Dutcher, W. 1901. Results of special protection to gulls and terns
obtained through the Thayer Fund. Auk 18(2):76-103.
Dutcher, W. 1904. Report of the A.O.U. Committee on the Protection
of North American Birds for the year 1903. Auk 21(suppl.):97-208.
Emison, W. B., F. S. L. Williamson, and C. M. White. 1971.
Geographical affinities and migrations of the avifauna on
Amchitka Island, Alaska. BioScience 21(12):627-631.
Fay, F. H., and T. J. Cade. 1959. An ecological analysis of the
avifauna of St. Lawrence Island, Alaska. Univ. Calif. Publ. Zool.
63:73-150.
Fernald, M. L. 1925. Persistence of plants in unglaciated areas of
boreal America. Mem. Am. Acad. Arts Sci. 15:239-342.
Fisher, J. 1952. The fulmar. Collins, London. 496 pp.
Fisher, J., and R. M. Lockley. 1954. Seabirds: An introduction
to the natural history of the seabirds of the North Atlantic.
Houghton Mifflin Co., Boston. 320 pp.
Fisher, J., and H. G. Vevers. 1943. The breeding distribution,
history and population of the North Atlantic gannet _(Sula
bassana)_. Part I. A history of the gannet's colonies, and the
census in 1939. J. Anim. Ecol. 12:173-213.
Fisher, J., and H. G. Vevers. 1944. The breeding distribution,
history and population of the North Atlantic gannet _(Sula
bassana)_. Part II. The changes in the world numbers of the
gannet in a century. J. Anim. Ecol. 13:49-62.
Flegg, J. J. M. 1972. The puffin on St. Kilda 1969-71. Bird Study
19:7-17.
Forbush, E. H. 1929. Birds of Massachusetts and other New England
States. Vol. I. Massachusetts Department of Agriculture, Boston.
481 pp.
Fordham, R. A. 1968. Dispersion and dispersal of the Dominican gull
in Wellington, New Zealand. Proc. New Zeal. Ecol. Soc. 15:40-50.
Fordham, R. A. 1970. Mortality and population change of Dominican
gulls in Wellington, New Zealand, with a statistical appendix by
R. M. Cormack. J. Anim. Ecol. 39(1):13-27.
Frazer-Darling, F. 1938. Bird flocks and the breeding cycle.
Cambridge Univ. Press, Cambridge, England. 124 pp.
Gilpin, M. E. 1975. Limit cycles in competition communities. Am.
Nat. 109:51-60.
Gromme, O. J. 1927. Some highlights on the faunal life of the
Alaskan Peninsula. Milw. Public Mus. Yearb. 7:30-45.
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.
Harrington, B. A. 1974. Colony visitation behavior and breeding
ages of sooty terns _(Sterna fuscata)_. Bird-Banding
45(2):115-144.
Harris, M. P. 1964. Aspects of the breeding biology of the
gulls _Larus argentatus_, _L. fuscus_ and _L. marinus_. Ibis
106(4):432-456.
Harris, M. P. 1976. The present status of the puffin in Britain and
Ireland. Brit. Birds 69(7):239-264.
Harris, M. P., and W. J. Plumb. 1965. Experiments on the ability
of herring gulls _Larus argentatus_ and lesser black-backed
gulls _L. fuscus_ to raise larger than normal broods. Ibis
107(2):256-257.
Hickey, J. J., editor. 1969. Peregrine falcon populations--their
biology and decline. Univ. Wisconsin Press, Madison. 596 pp.
Hildén, O. 1965. Habitat selection in birds: a review. Ann. Zool.
Fenn. 2(1):53-75.
Holdgate, M. W., editor. 1971. The sea bird wreck in the Irish Sea,
autumn 1969. Nat. Environ. Res. Council Publ. Ser. C, No. 4. 17
pp.
Hultén, E. 1937. Outline of the history of arctic and boreal biota
during the Quaternary period. Bokforlags Aktiebolaget Thule,
Stockholm. 168 pp.
Hunt, G. L. 1972. Influence of food distribution and human
disturbance on the reproductive success of herring gulls. Ecology
53(6):1051-1061.
Jones, R. D. 1970. Reproductive success and age distribution of
black brant. J. Wildl. Manage. 34(2):328-333.
Kadlec, J. A. 1971. Effects of introducing foxes and raccoons on
herring gull colonies. J. Wildl. Manage. 35(4):625-636.
Kadlec, J. A., and W. H. Drury. 1968. Structure of the New England
herring gull population. Ecology 49(4):644-676.
Kenyon, K. W., and R. E. Phillips. 1965. Birds from the Pribilof
Islands and vicinity. Auk 82(4):624-635.
Klein, D. R. 1959. Saint Matthew Island reindeer-range study. U.S.
Fish Wildl. Serv., Spec. Sci. Rep.--Wildl. 43. 48 pp.
Kluyver, H. N. 1951. The population ecology of the great tit,
_Parus major_ L. Ardea 39:1-135.
Kluyver, H. N. 1966. Regulation of a bird population. Ostrich 38
(Suppl. 6):389-396.
Kluyver, H. N., and L. Tinbergen. 1953. Territory and the
regulation of density in titmice. Arch. Neér. Zool. 10:265-289.
Lack, D. 1948. Natural selection and family size in the starling.
Evolution 2:95-110.
Lack, D. 1954. The natural regulation of animal numbers. Clarendon
Press, Oxford. 343 pp.
Lack, D. 1964. A long-term study of the great tit _(Parus major)_.
J. Anim. Ecol. 33(Suppl.):159-173.
Lack, D. 1966. Population studies of birds. Clarendon Press,
Oxford. 341 pp.
Mackay, G. H. 1893. Observations on the breeding habits of _Larus
atricilla_ in Massachusetts. Auk 10(4):333-336.
Manuwal, D. A. 1974. Effects of territoriality on breeding in a
population of Cassin's auklet. Ecology 55(6):1399-1406.
May, R. M., and W. J. Leonard. 1975. Nonlinear aspects of
competition between species. SIAM J. Appl. Math. 29(2):243-253.
Mills, J. A. 1973. The influence of age and pair bond on the
breeding biology of the red-billed gull _Larus novaehollandiae
scopulinus_. J. Anim. Ecol. 42:147-162.
Murphy, R. C. 1936. Oceanic birds of South America, Vols. I and II.
Am. Mus. Nat. Hist., New York. 1245 pp.
Murray, M. D., and R. Carrick. 1964. Seasonal movements and
habitats of the silver gull _Larus novaehollandiae_ Stephens in
southeastern Australia. CSIRO Wildl. Res. 9:160-188.
Nelson, J. B. 1966. Population dynamics of the gannet at Bass Rock,
with comparative information for other Sulidae. J. Anim. Ecol.
35:443-470.
Nettleship, D. 1972. Breeding success of the common puffin
(_Fratercula arctica_ L.) on different habitats at Great Island,
Newfoundland. Ecol. Monogr. 42:239-268.
Nicholson, A. J. 1933. The balance of animal populations. J. Anim.
Ecol. 2:132-178.
Nisbet, I. C. T. 1972. Disaster year for terns. Man and Nature,
Dec. 1972:16-21.
Nisbet, I. C. T. 1973. Courtship-feeding, egg-size and breeding
success in common terns. Nature 241:141-142.
Nisbet, I. C. T., and W. H. Drury. 1972. Post-fledging survival in
herring gulls in relation to brood-size and date of hatching.
Bird-Banding 43(3):161-172.
Noble, G. K., and M. Würm. 1943. The social behavior of the
laughing gull. Ann. N. Y. Acad. Sci. 45:179-200.
Norton, A. H. 1921. Report of the field agent for Maine. Bird-Lore
23:355-356.
Norton, A. H. 1924. Notes on birds of the Knox County region. Maine
Nat. 4:35-39.
Palmer, R. S. 1949. Marine birds. Harvard Bull. Mus. Comp. Zool.
102. 656 pp.
Perrins, C. 1965. Population fluctuations and clutch-size in the
great tit, _Parus major_ L. J. Anim. Ecol. 34:601-647.
Pitelka, F. A., P. Q. Tomich, and G. W. Treichel. 1955. Ecological
relations of jaegers and owls as lemming predators near Barrow,
Alaska. Ecol. Monogr. 25:85-117.
Preble, E. A., and W. L. McAtee. 1923. A biological survey of the
Pribilof Islands, Alaska. U.S. Fish. Wildl. Serv., N. Am. Fauna
46:1-255.
Reed, A., and J. G. Cousineau. 1967. Epidemics involving the common
eider _(Somateria mollissima)_ at Ile Blanche, Quebec. Nat. Can.
(Que.) 94:327-334.
Sealy, S. G., F. H. Fay, J. Bédard, and M. D. F. Udvardy. 1971. New
records and zoogeographical notes on the birds of St. Lawrence
Island, Bering Sea. Condor 73(3):322-336.
Serventy, D. L. 1967. Aspects of the population ecology of the
short-tailed shearwater _Puffinus tenuirostris_. Proc. Int.
Ornithol. Congr. xiv:165-190.
Sladen, W. J. L. 1966. Additions to the avifauna of the Pribilof
Islands, Alaska, including five species new to North America. Auk
83:130-135.
Soots, R. F., Jr., and J. F. Parnell. 1975. Ecological succession
of breeding birds in relation to plant succession on dredge
islands in North Carolina estuaries. N.C. Sea Grant Publ.
UNC-SG-75-27, Raleigh.
Thompson, M. C., and R. L. DeLong. 1969. Birds new to North America
and the Pribilof Islands, Alaska. Auk 86(4):747-749.
Tickell, W. L. N. 1968. The biology of the great albatrosses,
_Diomedea exulans_ and _Diomedea epomorpha_. Antarct. Res. Ser.
12:1-55.
Tuck, L. M. 1960. The murres: their distribution, populations and
biology. Can. Wildl. Serv., Rep. Ser. No. 1. 260 pp.
Uspenski, A. M. 1956. The bird bazaars of Novaya Zemlya. U.S.S.R.
Acad. Sci., Moscow. (Translated from Russian.) Canad. Wildl.
Serv. Transl. Russian Game Rep. 4. 159 pp.
Vermeer, K. 1963. The breeding ecology of the glaucous-winged gull
_(Larus glaucescens)_ on Mandarte Island, B.C. Occas. Pap. B. C.
Prov. Mus. 13:1-104.
Wynne-Edwards, V. C. 1959. The control of population-density
through social behaviour: a hypothesis. Ibis 101:436-441.
Time-Energy Use and Life History Strategies of Northern Seabirds
by
Erica H. Dunn
Long Point Bird Observatory
Point Rowan, Ontario, Canada
Abstract
Time and energy budgets can be compared
among species of birds with very different
ecology as a way of summarizing differences
and as an approach to determining selective
pressures on each species. This paper reviews
time-energy use of northern seabirds. Energetic
cost of maintenance (basal metabolism,
thermoregulation, and procurement and
processing of food) depends largely on the
following factors: (1) small birds have higher
metabolic costs per unit size than do larger
ones; (2) body structure affects the cost of
locomotion as well as of food procurement; (3)
climate affects metabolic costs; and (4) food
availability and nutrition vary among food
types, and throughout the year within a food
type. Little is known of maintenance energetics
in seabirds. Time and energy allocations
to items beyond basic maintenance are also
compared. Patterns and costs of molt and
migration are known only in a general way, and
the variety of possible patterns suggests that
more research would be of value. Almost nothing
is known of location and daily activities of
seabirds outside the breeding season. The
review of breeding season activities is more
comprehensive, and stresses the variety of
factors known to affect timing, and the total
time devoted to and the energetic costs of
various aspects of reproduction. Some of these
factors are weather, year, geographic location,
feeding conditions, age, sex, and distance
of food source from the breeding colony.
Species characteristics such as clutch size,
egg and yolk size, developmental type, growth
rate, food type, and behavior combine with
environmental variables to make seabirds a very
diverse group in time and energy budgeting.
Time-energy studies and determination of
productive energy (energy remaining after
maintenance needs have been met) can be useful
in pinpointing those groups of birds and the
times of year when birds are most vulnerable
to environmental stress. Life history
considerations suggest that most seabirds are
adapted to low population turnover and would
not be able to recover quickly from sudden
increases in mortality.
Effective management of a population requires manipulation of the
factors most critical in causing population increase or decrease.
Deciding what these factors are and which are most suitable for
effective manipulation is very difficult due to the complexity of life
cycles and possible factors affecting demography. It takes a thorough
knowledge of a species and of its relationships with the biotic and
abiotic environment to make effective management decisions. The
following review of seabird time and energy use is meant to emphasize
the wide variation of species ecology within this avian group.
Time and energy patterning is being used as the basis of ecological
comparison for the following reason. Any activity of an animal requires
time and energy use; therefore, the patterning of use makes a common
thread to which allocation to all activities in a bird's life cycle
can be related. Time-energy patterns can be compared among birds with
diverse food types, habitats, life cycles, and life expectancy, and
therefore offer an opportunity for comparison not available through
other kinds of analysis (King 1974).
The amounts of time and energy allocated by an organism to different
aspects of survival and reproduction should be regarded as being molded
by natural selection to optimize (not necessarily to maximize) lifetime
reproductive output (Fisher 1958; Williams 1966; Schoener 1971). Thus,
differences in time and energy use between species should reflect
adaptation to different biotic and abiotic environments. By comparing
time and energy use, one can gain insight into the selective pressures
on each species and have a basis on which to compare complex ecology
more meaningfully than if one listed other types of differences.
This review of time-energy use in northern seabirds cannot be
comprehensive, largely because many of the necessary data are lacking.
It stresses major areas of difference, however, and points out aspects
about which little is yet known.
Cost of Living
Every animal must expend a basic amount of energy on normal
maintenance, excluding activities normally allocated to a relatively
narrow time span, such as reproduction. This "existence energy"
expenditure consists of basal metabolism, thermoregulation, and the
costs of gathering and processing food, and could also be referred to
as the animal's basic "cost of living." In discussing the components
of the cost of living, energy use is emphasized and time largely
ignored--partly because metabolism occurs irrespective of time (it is
not something the animal can turn off for a period) and partly because
time use in normal maintenance and foraging has been little studied.
_Metabolism_
Basal metabolic rate (BMR) depends greatly on body size (Lasiewski and
Dawson 1967; Zar 1968), and the costs per unit size are higher for a
small bird than for a large one (Fig. 1). The BMR is somewhat lower in
seabirds and other nonpasserines than in passerines of similar size
(Dawson and Hudson 1970).
[Illustration: Fig. 1. Energy cost of various metabolic functions
in relation to body size in birds. "0° Existence" refers to total
metabolic costs of caged birds held at 0°C. From Calder (1974).]
The relationship between BMR and body size is paralleled by that
between size and other metabolic costs, such as for thermoregulation
at a given temperature and for activity (Fig. 1; Kendeigh 1970; Tucker
1970; Schmidt-Nielsen 1972; Berger and Hart 1974; Calder 1974). Basal
metabolic rate can therefore be used as an index of the overall cost of
living as far as metabolic functions are concerned. Small birds must
allocate a greater proportion of their energy resources than larger
ones to merely staying alive, and have a higher cost of living.
The suggestion in Fig. 1 that it is easy to measure activity costs in
a straightforward manner is misleading, because the figure represents
measures taken under standard conditions. Factors known to affect the
cost of flight, for example, include anatomical adaptations (such
as wing loading and wing shape), the type of flight (ascending,
descending, gliding), and the speed of flight (Fig. 2; Tucker 1969,
1974; Hainsworth and Wolf 1975). The cost of a series of short flights
may be higher than that for a long one because of the extra energy
required for takeoff and landing. A few estimates have been made for
the cost of flight, mostly in birds moving almost constantly (Lasiewski
1963; Nisbet 1963; Tucker 1972, 1974; Utter and LeFebvre 1970; Berger
and Hart 1974), but the methods may be inadequate for birds that fly
short distances frequently.
[Illustration: Fig. 2. Energy cost of flying at different speeds
and angles as compared with basal metabolic rate (BMR). Solid
lines and solid circle refer to flight cost and BMR for budgerigar
_(Melopsitticus undulatus)_. Dashed line and open circle refer to
flight cost and BMR of the laughing gull. From Tucker (1969).]
Little work has been done on the cost of locomotion in seabirds: that
of Eliassen (1963) on great black-backed gulls _(Larus marinus)_,
Berger et al. (1970) on ring-billed gulls _(L. delawarensis)_, and
Tucker (1972) on the laughing gull _(L. atricilla)_, and indirect
calculations of soaring flight characteristics in albatrosses,
_Diomedea_ spp. (Cone 1964), and the fulmar, _Fulmarus glacialis_
(Pennycuick 1960). Swimming has been shown to be more costly than
flying in ducks (Schmidt-Nielsen 1972) and may be for seabirds as well.
More energy is also probably used in underwater swimming than in flying.
The energetic costs of thermoregulation under natural conditions
are not easy to estimate. Thermal energy is gained from and lost
to the environment, and the degree of exchange depends not only
on air temperature but also on metabolic rate, insulation, body
temperature, posture, humidity, convection, and radiation. Radiation,
in turn, depends on cloud cover, shade, and reflective and absorptive
characteristics of the organism and of the environment (Porter and
Gates 1969; Calder and King 1974). Most of these quantities are
changing constantly, and insulation and metabolic rate may vary on a
seasonal basis with acclimation (Dawson and Hudson 1970).
At present, no direct measurement technique exists for determining
natural thermoregulatory costs, although a few estimates have been made
(King 1974), including several for seabird nestlings (Dunn 1976_a_,
1976_b_ for double-crested cormorants, _Phalacrocorax auritus_,
and for herring gulls, _Larus argentatus_). For most birds, the
temperature environment actually faced over a year's time has never
been measured, and for no bird has a full description of the complete
thermal environment been made. It is clear that climate and degree
of exposure are important elements in the basic cost of living, and
that thermoregulatory costs average higher in small birds than in
larger ones, but beyond that little information is available. Work on
thermoregulatory costs of free-living chicks of two species of seabirds
suggests that insulative properties can lead to marked differences in
the metabolic costs of different species in an essentially identical
environment (Dunn 1976_a_, 1976_b_).
_Food Procurement and Processing_
Gathering and processing food is another major component of the cost
of living. Both the nutritional value of food and its availability (a
rather vague term covering both abundance and ease of capture) are
extremely diverse and variable, making estimations of foraging cost and
benefit difficult (Ashmole 1971; Fisher 1972; Sealy 1975_a_).
Availability of food varies throughout the year, particularly in
marine invertebrates that form the diet of many seabirds (e.g., Spaans
1971; Bédard 1969_a_). High arctic oceans have a very high peak of
productivity in the summer, whereas the low arctic has a lower, but
longer-lasting, peak (Ashmole 1971). Fish stocks increase in summer as
well (Snow 1960; Pearson 1968; Sealy 1975_a_), and decline or disperse
in autumn (Potts 1968). Catch-ability may also differ widely from year
to year (e.g., E. K. Dunn 1973).
Marine foods are likely to have a patchy distribution, which may make
food stocks difficult to locate, even in times of abundance (Ashmole
1971; Sealy 1975_a_). Birds in localities with low food abundance
frequently show alterations in time and pattern of foraging, sometimes
even changing diets (Cramp 1972; Henderson 1972; Hunt 1972; Lemmetyinen
1972). The time and energy expended in finding and capturing food
by different seabird species must vary widely according to the form
of foraging used: plunge-diving, beach scavenging, aerial robbing,
underwater pursuit, and so on. Even when different species have
traveled the same distance to an identical food stock, therefore, the
costs of procurement differ.
Time and energy spent foraging depends not only on abundance and ease
of capture, but also on nutritional return, and on the age and size of
the bird. Fig. 3 shows that the smaller species in a seabird community
may spend the most time foraging. Even though this illustration is
taken from the breeding season when food demands of the young must be
taken into account, it suggests a difference based on cost of living
according to size.
[Illustration: Fig. 3. Time spent foraging in the breeding season as a
function of body size. From Pearson (1968). AT = arctic tern _(Sterna
paradisaea)_, CT = common tern _(S. hirundo)_, ST = sandwich tern
_(Thalasseus sandvicensis)_, K = black-legged kittiwake, P = common
puffin, M = common murre, LBB = lesser black-backed gull, S = shag.]
Age of the bird affects time and energy commitment to foraging because
younger birds are often less skilled at capturing food. This has been
noted particularly in long-lived seabird species (Orians 1969; Dunn
1972; LeCroy 1972; Buckley and Buckley 1974; Barash et al. 1975). Older
juveniles may be excluded from feeding areas by more experienced,
territorial adults (Moyle 1966), whereas immatures are not (Drury and
Smith 1968; Ingolfsson 1969).
Nutritional and energetic return obtained from food is a very important
factor in foraging strategy that has not received the attention it
deserves. Table 1 lists the caloric value of various foodstuffs and
illustrates how little is known about foods eaten by seabirds. Although
caloric content and abundance of food have often been accepted as the
most important determinants of foraging strategies (Bookhout 1958;
Emlen 1966; West 1967; Bryant 1973), they may frequently be less
important than nutritional value and digestibility, also shown in Table
1 (Pulliam 1974).
Since fish seem to be highly digestible, most of the energy contained
in them is available to the consumer. There are, unfortunately, no data
on the digestibility of marine invertebrates, but those for insects
suggest that digestibility, at least of crustaceans with exoskeletons,
is somewhat lower than that for fish. A bird would therefore have to
eat a larger biomass of invertebrates than of fish to satisfy the same
energetic needs (although cost of procurement might not be as high as
for fish).
Table 1. _Nutritional value of foods eaten by birds._ After data
in Hunt (1972) and E. H. Dunn (1973).
A: Kcal/g fresh wt.
B: Digestive efficiency
C: Kcal metabolizable energy/g fresh wt.
------------------------------------------------------------------------------
Percent fresh wt.
composed of:
----------------------
Food type A H₂O Fat Protein B C
------------------------------------------------------------------------------
Vegetable 1.2-5.2 59-86 0.4-3 3-5 30-32 0.3-2.3
Tropical fruits 1.2 75 8 1
Various seeds 4.0-7.3 3-13 1-40 10-29 76-80 3.0-5.2
Various insects 1.4-5.2 65-75 1-3 9-18 66-69 0.9-3.5
Whiting (fish) 1.1 81 79 0.9
Various freshwater fishes 1.2 75 5 18 81
Mix of fish eaten by
double-crested cormorants 1.1 74 1 16 82 0.9
on NE coast
Fresh herring and mackerel 1.9 67 13 19
Garbage ("average" mix) 1.5 67 8 19
Crab with eggs 1.0 68 5 1
Euphausid shrimp 0.8 80 2 1
Clam (edible part only) 0.8 80 1 13
------------------------------------------------------------------------------
A bird must satisfy not only energetic needs, but also nutritional
requirements. Fish are high in protein (Table 1), but what little is
known of marine invertebrates suggests a low proportion of protein in
relation to total bulk. Protein is vital to growth of nestlings (Fisher
1972; Lemmetyinen 1972), and 4-8% protein in the diet seems to be
required for minimal maintenance of adults (Martin 1968; Fisher 1972).
Some seabirds (such as puffins, _Fratercula_) that eat a varied diet
raise their young exclusively on fish (Bédard 1969_b_; Nettleship 1972;
Sealy 1973_a_).
Other aspects of nutrition, such as vitamins and minerals, are also
important to avian health (Brisbin 1965; Fisher 1972). To further
complicate matters, nutritional values vary with season, as do birds'
requirements for them (Myton and Ficken 1967; Moss 1972). Adults must
adjust their time and energy allocation to foraging to optimize not
only energetic, but also nutritional return.
Optimal time and energy allocation has been studied in theory (Orians
1971; Schoener 1971; Pulliam 1974; Katz 1974) and some direct
observations have been carried out, largely on seedeaters (Bookhout
1958; Myton and Ficken 1967; Royama 1970; Moss 1972; Willson 1971;
Willson and Harmeson 1973). The direct studies, in particular,
point out the basic importance of studying cost-benefit ratios by
interrelating complex factors of food availability, searching patterns,
and type, size, and caloric and nutritional value of foods.
Time-energy Use Beyond the Cost of Living
This section concerns variation in time and energy allocated
by seabirds to activities above and beyond the cost of
living--particularly to migration, molt, and reproduction. Allocation
to such items as avoidance of predation and competition is not
considered here, because they are not readily analyzed as activities
to which time and energy are devoted in a specific part of the annual
cycle.
The previous discussion dwelt on energy considerations and could have
referred to almost any group of birds. The following treatment centers
on time use of northern seabirds. Little is known of energetics beyond
the cost of living, although estimates have been made for certain
aspects of migration, molt, and reproduction (Nisbet 1963; Hussell
1969; Hart and Berger 1972; Payne 1972; Ricklefs 1974). Essentially
nothing is known, however, of the relationship of such costs to the
amount of energy available to the bird once basic maintenance costs
have been met (productive energy). Because such complete data are not
available, the following account dwells largely on variation in timing
and total time devoted to activities beyond basic maintenance.
[Illustration: Fig. 4. Typical patterns of generalized annual cycles
in reproduction, migration, and wing molt in northern seabirds. Solid
line shows reproductive season, dotted line the period of migration
or dispersion, and dashed line the period of annual primary molt.
Data from Dorst (1961), Stresemann and Stresemann (1966), and Ashmole
(1971).]
_Migration_
Among northwestern North American seabirds, most coastal feeders, such
as gulls, cormorants, and many alcids and petrels, have only a short
southward migratory movement, and many others are more or less resident
(Dorst 1961; Ashmole 1971). Terns, on the other hand, migrate long
distances in a short time to places where small fish are available
near shore in the winter. Other long-distance migrants--Sabine's gull
_(Xema sabini)_, jaegers (_Stercorarius_ spp.), pelagic phalaropes
(_Phalaropus_, _Lobipes_), and kittiwakes (_Rissa_ spp.)--tend to
scatter widely over the southern ocean, concentrating near areas of
upwelling (Dorst 1961; Ashmole 1971). Groups such as murres (_Uria_
spp.), eiders (_Somateria_ spp.), and grebes (_Podiceps_ spp.) may
move considerable distances by swimming (Dorst 1961; Tuck 1960). True
migration tends to take place directly before and after reproduction,
whereas dispersal or nomadism takes place over a long period of the
winter (Fig. 4).
Among species remaining in the northern hemisphere, younger birds
frequently disperse greater distances than do breeding adults (Coulson
1961; Kadlec and Drury 1968; Southern 1967), and the degree of
dispersal can vary among colonies of the same species (Coulson and
Brazendale 1968).
Energy costs of migration must vary according to distances covered
and amount of time allocated to migration. Aside from the references
to cost of flight mentioned earlier, however, migratory costs have
scarcely been studied. Dolnik (1971) has estimated that chaffinches
_(Fringilla coelebs)_ expend about as much energy migrating south as
they would on thermoregulation if they overwintered on their breeding
grounds. Long-distance migration is presumably selected because the
birds are able to collect food more efficiently, because the risks of
death or injury in migrating are less than in residency, and so on.
Interspecific and intraspecific competition may also be involved (Cox
1968). In other words, migratory patterns are selected to optimize
survival and reproduction in alternating environments (Cohen 1967;
Drury and Nisbet 1972).
Table 2. _Wing molt in alcids._ After Stresemann and Stresemann
(1966).
---------------------------------------------------------------------
Rapidity of wing molt Timing of start of molt Species
and (indented) flight
capability in molt
Slow Retained During care of young Cassin's auklet,
parakeet auklet
_(Cyclorhynchus
psittacula)_,
whiskered auklet
_(Aethia pygmaea)_
Retained After young become Least auklet
independent _(A. pusilla)_,
crested auklet _(A.
cristatella)_
Rapid Poor After arrival in Marbled murrelet,
winter quarters Kittlitz's murrelet
_(Brachyramphus
brevirostris)_
Almost synchronous None After end of breeding Xantus' murrelet
_(Endomychura
hypoleuca)_
Synchronous None As soon as young go to Guillemots (_Cepphus_
sea spp.), murres,
razorbill _(Alca
torda)_, dovekie
_(Alle alle)_
None In winter, after body Puffins
molt
---------------------------------------------------------------------
Although one may suspect that location of winter food supply is the
main environmental factor affecting migratory patterns, there is little
direct evidence on the reasons for, or the benefits accruing from,
the different patterns seen in seabirds. Study of cost-benefit ratios
of foraging in different stages of migration might help clarify the
question.
_Molt_
Patterns of molt vary widely among seabirds. The commonest pattern is
for a prenuptial body molt to occur in spring, and for an extended wing
molt to begin after the breeding season and continue well into the
winter (Fig. 4). In short-distance migrants, molt may overlap slightly
with the end of breeding and can last up to 6 months, as in most gulls,
terns, alcids, nonmigratory jaegers, and cormorants (Stresemann and
Stresemann 1966).
Long-distance migrants frequently delay molt until in the winter
quarters (lesser black-backed gull, _Larus fuscus_; Sabine's gull;
jaegers; arctic tern, _Sterna paradisaea_; and marbled murrelet,
_Brachyramphus marmoratus_) and molt there may occur rapidly (3.5
months in the arctic tern). Certain other long-distance migrants
begin molt before leaving the breeding grounds (herring gull; skua,
_Catharacta skua_; Leach's petrel, _Oceanodroma leucorhoa_; and
fulmar), although molt may be interrupted during migration, as in
_Larus argentatus heuglini_ (Stresemann and Stresemann 1966). Duration,
timing, and rapidity of molt are particularly varied among the alcids
(Table 2).
A few unusual molt patterns are found in northern seabirds. The ivory
gull _(Pagophila eburnea)_ has its major annual wing and body molt
immediately before it breeds. In several other species such as the
glaucous gull _(Larus hyperboreus)_ and Cassin's auklet _(Ptychoramphus
aleuticus)_ the molt almost completely overlaps the reproductive cycle
(Johnston 1961; Payne 1965). Potts (1971) documented a molt pattern in
shags _(Phalacrocorax aristotelis)_ which is more typical of tropical
seabirds. Several cycles of wing molt take place simultaneously, each
lasting more than a year, and molt ceases in winter. By the time
breeding age is reached, each flight feather is replaced once a year.
Within these broad categories of molt pattern there are sometimes
variations according to age, sex, and even subspecies (Stresemann and
Stresemann 1966). Male common eiders _(Somateria mollissima)_ molt
directly after mating, when their reproductive role is completed,
whereas females molt only after they have taken their young to sea.
Nonbreeders and failed breeders frequently begin molt while other
adults are still raising young and not molting--e.g., many alcids,
gulls, storm-petrels, and fulmars (Stresemann and Stresemann 1966;
Ingolfsson 1970; Harris 1971; Harris 1974; Sealy 1975_b_). In ivory
gulls, which molt just before reproduction, and in Sabine's gulls,
which complete molt just before breeding, nonbreeders may extend wing
feather growth into the breeding season (Stresemann and Stresemann
1966).
There is little information on the energetic cost of molt, although
there are indications of at least some expense. Belopol'skii (1961)
showed that nonmolting seabird species tended to gain weight after
reproduction, whereas those that immediately started molt tended to
lose weight. Among other birds, however, it is common for individuals
to gain weight just before, and even during molt (Payne 1972). The BMR
is known to rise in molting birds (Blackmore 1969; Lustick 1970; Payne
1972), from as little as 5% to as much as 34% above nonmolting levels.
In one study, about 35-40% of the increased BMR represented extra
thermoregulatory costs incurred by lessening of insulation and increase
in heat loss from well-vascularized new feathers; the rest of the
increase represented the energetic cost of growing feathers (Gavrilov
1974). The fact that molt rarely overlaps with breeding suggests that
the energetic cost, even if slight, may be incompatible with the
already high costs of reproduction (Payne 1972). Cassin's auklets,
which do molt while breeding, may cease molt while feeding large young
(Payne 1965), and certain species interrupt molt during migration
(Stresemann and Stresemann 1966). Doubtless a rapid simultaneous molt
is more costly than a long gradual one.
Rapid molt appears to occur at a time in the annual cycle when food
resources are abundant (spring or late summer), whereas extended molt
generally occurs over winter (e.g., Bédard 1969_a_). If one speculates
that energy availability is the main determinant of molt patterns,
one can also speculate on the cause behind some of the more unusual
patterns. Possibly birds in which molt and breeding overlap either have
extraordinary available energy at that time or else face shortages
in other periods. For example, ivory gulls, which breed in the high
Arctic, molt when food resources have become abundant in the low Arctic
but before the high Arctic breeding grounds have thawed sufficiently
for reoccupation.
Speed of molt may also reflect availability of energy resources or
of nutrients needed for feather growth (Payne 1972), but must also
be influenced by the need for full flight capabilities to obtain
food. The eider duck and many alcids that shed wing feathers almost
simultaneously do not need their wings for flight after the young have
left the breeding colony. Hydrodynamic considerations suggest that
their fishing capabilities may even be improved (Storer 1960). This is
not true for the smaller species--e.g., _Aethia_ molts only one feather
at a time and retains full flight capabilities (Table 2). Climate may
also influence simultaneity of molt if heat loss in rapid molt is
particularly severe.
_Reproduction_
Time use of seabirds is best known for the reproductive period, when
the birds are on relatively accessible breeding grounds, the weather is
most suitable for observation, and academic researchers are freed from
their jobs. Even so, the details of timing are known for only a few of
the species and localities on the northwest North American coast (e.g.,
Drent and Guiguet 1961; Drent et al. 1964; Cody 1973; Sealy 1973_a_,
1975_b_, 1975_c_). The following discussion emphasizes the multitude
of environmental factors known to influence timing and total length of
time devoted to various aspects of the reproductive cycle.
Timing of the Season
Each species of seabird returns to the colony site when weather
conditions have ameliorated sufficiently to meet its particular needs.
For example, the early arrivals to islands in the Barents Sea are
murres, kittiwakes, and herring gulls, which need only small cracks in
the sea ice to meet their feeding requirements (Belopol'skii 1961).
Eiders in North America also return early, when a few ice leads have
formed (Schamel 1974). Common puffins _(Fratercula arctica)_ and mew
gulls _(Larus canus)_ are somewhat later arrivals, and terns and a few
parasitic jaegers _(Stercorarius parasiticus)_ are the latecomers to
Barents Sea colonies (Belopol'skii 1961).
The timing of the season (as illustrated in Fig. 5) varies widely
among localities, and because of local weather patterns and ocean
currents, this variation can be unrelated to latitude (Belopol'skii
1961). Examples of such variation are also known in North America: for
instance, Leach's storm-petrels in Alaska lay eggs 2 to 3 weeks later
than do those in California (Harris 1974); however, the details of
timing are largely unknown for many species in this region. Progression
of thaw, which also varies from year to year, causes variation in the
timing of the breeding season (Belopol'skii 1961; Evans and McNicholl
1972). Fig. 6 shows the diversity in start of the breeding season for
different species on the same island in the Barents Sea as well as
variation in time devoted to various components of the reproductive
cycle.
[Illustration: Fig. 5. Differential average arrival on breeding grounds
and average duration of prenesting period of thick-billed murres
_(Uria lomvia)_ and black-legged kittiwakes on various colonies in the
Barents Sea. From Belopol'skii (1961). Length of prenesting period in
days (shaded bars) indicated on right. Letters represent locations as
follows: A = Novaya Zemlya, Kara Straits; B = Novaya Zemlya, Karmakuly
Bay; C = Franz Josef Land; and D = East Murman.]
Prenesting Activities
Some species are apparently able to delay maturity of sexual organs
until environmental conditions are suitable for nesting--e.g., burrow
and crevice nesters in the Barents Sea do not become sexually mature
until snowmelt (Belopol'skii 1961). Many others, however, reach sexual
maturity soon after arrival on the breeding grounds, and a few (such as
jaegers and kittiwakes) mature in migration or on the wintering grounds
(Belopol'skii 1961). Northern phalaropes _(Lobipes lobatus)_ sometimes
lay eggs as early as 1 week after arrival (Hilden and Vuolanto 1972).
This factor, in combination with timing of arrival, affects the amount
of time spent in prenesting activities (Fig. 6). Most species gain
weight during this period (Belopol'skii 1961), and the time required
for each species to reach full breeding condition must also depend on
feeding conditions and the state of the bird on its arrival at the
nesting site. These factors help explain why early arriving species are
not necessarily early nesters (Fig. 6).
[Illustration: Fig. 6. Variation in timing of events in the
reproductive cycle of Barents Sea seabirds nesting on the same island.
Data from Belopol'skii (1961). Shaded bars at left indicate the
prelaying periods, open bars the incubation periods, and shaded bars at
right the portion of the growth period in which the chick remains at
the nest site. Total length of time indicated is about 6 months.]
Aside from nest building, most prenesting activity consists of
courtship and territorial behavior. These activities have been well
described for representative seabird species, but because assessments
of time and energy devoted to them have been almost completely
neglected, they are not discussed further here. For examples, see
accounts in Gross (1935) for Leach's storm-petrel; Tinbergen (1935),
Bengtson (1968), Höhn (1971), and Howe (1975) for phalaropes; Storer
(1952) for common murre, _Uria aalge_, and black guillemot, _Cepphus
grylle_; Tschanz (1959) for common murre; Brown et al. (1967) for
Sabine's gull; Tinbergen (1960) for herring gull; McKinney (1961) for
eiders; Snow (1963) for shag; Thoresen (1964) for Cassin's auklet;
Vermeer (1963) and James-Veitch and Booth (1974) for glaucous-winged
gull _(Larus glaucescens)_; and Andersson (1973) for jaegers.
Nest Building
Although many northern seabirds have essentially no nest, they may
spend considerable time working or displaying at the site (Belopol'skii
1961). Black-legged kittiwakes _(Rissa tridactyla)_ have substantial
nests, but they are built in a comparatively short time (about a week)
soon after the birds arrive (Fig. 6). Shags also have substantial
nests, but they are not completed until about 1 or 2 weeks before the
first egg is laid (Snow 1963). Herring gulls build smaller nests, 5
to 10 days before laying, although in the Far North they and glaucous
gulls may not start building the nest until the first egg is laid
(Belopol'skii 1961). The eider always begins preparing the nest when
the first egg is laid (Belopol'skii 1961; Schamel 1974), and terns
and skuas, which build no nests, choose their sites at that time.
Murres, which frequently lay their eggs directly on snow, choose
a site somewhat earlier and spend considerable time protecting it
(Belopol'skii 1961). Burrows may be dug within a period as short as 3
days for Leach's storm-petrel (Gross 1935) to one as long as several
weeks in Cassin's auklets (Manuwal 1974_a_). Overall, the prelaying
period is longer for burrow nesters than for those using crevices
(Sealy 1973_a_).
The amount of time and energy spent by the male and female in nest
building differs among species. In Leach's storm-petrel, the male digs
the burrow (Gross 1935), whereas in eiders, the nest is built entirely
by the female. In most seabird species, the sexes share in nest
construction, but roles may still be separated. For example, in shags
the male collects the nest material and the female builds the nest
(Snow 1963).
Egg Laying
Timing of egg laying is influenced not only by weather (Erskine 1972;
Sealy 1975_c_), but also by numerous biotic factors. Smith (1966)
showed that where glaucous gulls, herring gulls, and Thayer's gulls
_(Larus thayeri)_ breed in mixed colonies, the peak of sexual activity
and egg laying in Thayer's gull is about midway between the peaks for
the other two species (Fig. 7). In nearby colonies where herring gulls
are absent, however, the peak of sexual activity in Thayer's gulls is
delayed about a week, and activity continues for a significantly longer
period (Fig. 7).
[Illustration: Fig. 7. Timing of peak sexual activity (a combined
measure of egg laying and testes size) in colonies of arctic gulls of
different species composition. From Smith (1966).]
Annual variations in food supply also will affect the start of the
egg-laying season. Belopol'skii (1961) cited an example from the
Barents Sea in 1940 when a series of storms made it difficult for
certain seabirds to find food. Murres and kittiwakes, which were able
to catch fish, started reproductive activities on schedule. Gull
breeding was delayed, however, and egg laying began in force only after
fishing boats arrived and started discarding offal. Onset of egg laying
in great cormorants _(Phalacrocorax carbo)_ is correlated to April air
temperatures (Erskine 1972), and this may also be related to variations
in spring increase of food availability. In certain birds the breeding
season has been shown to start particularly early when food supplies
are unusually abundant (Högstedt 1974; Källender 1974), but this has
not yet been demonstrated in seabirds.
Lastly, age and sex of seabirds are known to affect the timing of
egg laying (e.g., Coulson and White 1960; Lack 1966); older, more
experienced birds tend to lay earlier than do younger ones. In shags,
males tend to breed progressively earlier as they increase in age, but
females do not (Snow 1963).
Contrary to the situation in passerines, seabirds tend to lay their
clutches with relatively large time intervals between eggs. Eggs may be
laid every 2nd or 3rd day in alcids, larids, sternids, stercorariids,
and phalacrocoracids (Lack 1968), but every day in phalaropes (Howe
1975). Inasmuch as clutch size in northern seabirds varies from one
to five or six, the length of the laying period varies widely among
species.
Energetic costs of egg laying depend on the actual caloric content
of the egg and the speed with which the ova are developed (Ricklefs
1974). The energy in the egg is contained mainly in the yolk, and yolk
size depends largely on the developmental pattern shown by the young
after hatching (Table 3). Precocial chicks are hatched at a relatively
advanced stage, are covered with down, and have open eyes, can maintain
reasonably homeothermic body temperature, and leave the nest site to
feed themselves after a few hours or days. At hatching, semiprecocial
chicks appear similar to precocial chicks, although they are slightly
less well developed (Ricklefs 1974; Dunn 1975_a_). In contrast to
precocial chicks, they remain at the nest site for some time, are fed
by their parents, and tend to grow rather rapidly (Ricklefs 1968).
Altricial nestlings hatch at a much less advanced stage of development.
They are naked, blind, helpless, essentially poikilothermic, and depend
completely on their parents for food and shelter. They usually remain
at the nest until full grown. Semialtricial chicks show somewhat
intermediate characteristics (Nice 1962).
Table 3. _Amount of yolk in eggs of different types of birds._
After Ricklefs (1974).
------------------------------------------------
Developmental Percent yolk
type (by weight)
------------------------------------------------
Precocial 30-60
Semiprecocial 25-30
Altricial 15-25
+----------------------------------------------+
The amount of yolk (and therefore energy) in an egg is positively
correlated to the degree of development at hatching (Table 3). The same
is true for egg size: altricial and semialtricial birds have smaller
eggs relative to adult body weight than do semiprecocial and precocial
birds (Fig. 8). Clutch size, however, is unrelated to energy content
of the eggs. For example, shags (which are altricial) and eiders
(precocial) have among the largest clutches of northern seabirds (four
to six eggs).
[Illustration: Fig. 8. Egg weight as a function of body weight in
various northern seabirds. Solid symbols represent precocial and
semiprecocial species, and open symbols altricial and semialtricial
species: solid circles, alcids; solid triangles, gulls, terns, and
jaegers; solid squares, eiders; open squares, cormorants and _Morus
bassanus_; and open circles, petrels. Data from Belopol'skii (1961);
Drent (1965); Schönwetter (1967); Lack (1968); Bédard (1969_a_); Cody
(1973); Sealy (1973_b_); Harris (1974); and Manuwal (1974_a_).]
The energetic cost of egg laying depends not only on caloric content
of the egg and clutch size, but also on speed of development.
Ricklefs (1974) has shown that the energetic cost per day of egg
laying can be calculated from the energy content of the yolk and
white, clutch size, the amount of follicular growth per day, and the
laying interval between eggs. The energy content of a single egg
(expressed as percentage of BMR) has been estimated as follows: 45
(altricial passerines), 103 (semialtricial raptors), 126 (precocial
galliformes), 180 (precocial ducks), 226 (precocial shorebirds), and
320 (semiprecocial gulls and terns). Gulls and terns thus have very
costly eggs, as well as a moderately high clutch size (three). However,
the development time for a single ovum in the herring gull is unusually
long--9 to 10 days (King 1973). Ricklefs (1974), who calculated the
energetic cost per day (expressed as percentage BMR), estimated the
cost of a clutch in gulls and terns (120% BMR per day) to be similar
to that for various groups of precocial birds (about 125-180% BMR per
day). Unfortunately, the data required for calculation of the average
energetic cost of a clutch are not available for other northern
seabirds.
For no species have all the additional factors influencing the
energetic cost of a clutch been taken into account. For example,
eggs in a clutch may vary in size (and caloric content) according to
sequence in the clutch (Preston and Preston 1953; Snow 1960; Coulson
1963; Coulson et al. 1969). Age has a definite effect on laying
energetics, as older birds lay larger eggs (Coulson and White 1958;
Snow 1960; Coulson 1963; Coulson et al. 1969) and lay larger clutches
(Coulson and White 1960; Snow 1960). They also lay, on average, earlier
in the season (Coulson and White 1958; Snow 1960; Coulson et al. 1969),
and eggs laid late in the season (whether by young birds or older ones
in re-nesting attempts) tend to be smaller and contain less energy. In
addition, egg quality can vary with food supply: Snow (1960) found eggs
to have more yolk in years when food was abundant than in years when
food was scarce.
Egg-laying costs are, of course, borne entirely by the female,
although males may contribute some time and energy toward egg laying
through courtship feeding (Ashmole 1971; Henderson 1972; Nisbet 1973).
Courtship feeding takes place in most lariforms but not in eiders,
phalaropes, or cormorants.
The time and energy expended on egg laying can be profoundly influenced
by the degree of nest destruction, since females usually lay a
replacement clutch if the loss of the first does not occur too late in
the season. Factors causing egg destruction are numerous, but among
the most important in the north is predation. As is shown in Table 4,
the degree of egg predation in common murres is correlated to degree
of exposure of the nest--so even such an unlikely sounding factor as
physical characteristics of the nest site can affect the average time
and energy expended on egg laying by a given species or population.
Genuine second clutches are occasionally laid by phalaropes (Hilden and
Vuolanto 1972) and Cassin's auklets (Manuwal 1974_a_).
Table 4. _Predation on nests of common murres according to degree
of exposure._ From Belopol'skii (1961).
--------------------------------------------
Nests destroyed by
Nest exposure predators (%)
-------------------------------------------
Completely hidden 3.2
Partly exposed 5.8
Largely exposed 13.6
Completely exposed 18.2
--------------------------------------------
In short, time and energy devoted to egg laying depend not only on the
species, but also on a multitude of other biotic and abiotic factors,
such as age, sex, degree of nest destruction, weather, other species
present, and feeding conditions.
Incubation
The total time devoted to incubation does not depend directly on
developmental type or egg size but differs markedly among families
(Lack 1968). Since incubation period seems to be closely linked to
fledging period, factors affecting growth rate (discussed later)
apparently affect incubation period as well.
Each species has a different incubation rhythm. In birds in which the
sexes share in incubation, the sexes exchange places at intervals that
differ widely among different birds: several hours in lariforms and
some alcids (Drent 1965; Lack 1968; Preston 1968; Drent 1970); about
4 h in shags (Snow 1963); up to 11 h in the ivory gull (Bateson and
Plowright 1959); up to 24 h in certain other alcids (Manuwal 1974_a_;
Sealy 1975_a_); 33 h (on the average) in common puffins (Myrberget
1962); 72 h in ancient murrelets, _Synthliboramphus antiquus_ (Sealy
1975_a_); and 96 h in Leach's storm-petrel (Gross 1935). Degree of
attentiveness once a bird is on the nest also varies. Petrels may leave
the egg for several days (Gross 1935), whereas herring gulls cover
their eggs 98% of the time (Drent 1970).
The sexes share in incubation in most seabirds (Snow 1960; Drent 1965,
1970; Bédard 1969_a_), although females frequently take on the greater
role (Belopol'skii 1961). Only male phalaropes incubate the eggs, and
only female eiders. Eider hens do not feed during the entire incubation
period (25 days) and leave the nest only for short periods of about 10
min (Belopol'skii 1961; Schamel 1974).
Several methods exist for calculating the amount of heat input
necessary for normal development of a clutch of eggs (Ricklefs 1974).
There is controversy, however, as to whether an adult can provide
this warmth from excess body heat lost during the course of normal
metabolism or whether the adult must raise its metabolic level to
produce extra heat (Kendeigh 1973; King 1973; Ricklefs 1974). Several
studies of incubating birds suggest that, in at least some situations,
adults need not raise metabolic levels, but in others (large clutch,
severe weather), they probably do (Ricklefs 1974). Drent (1972)
estimated that herring gulls raise metabolic levels to a significant
degree during incubation.
In spite of the lack of quantitative data, one can surmise that the
cost of incubation varies among seabirds. Precocial and semiprecocial
birds tend to have a larger clutch weight relative to body weight
than do altricial birds (Fig. 8; Lack 1968), and therefore require
greater heat input to the eggs. These costs may be reduced by heavily
insulating the nest (e.g., eiders), or by nesting in burrows, which
have much more moderate and even climates than do external nests
(Richardson 1961; Manuwal 1974_a_). Other semiprecocial species,
however, such as the murre, may sometimes lay eggs directly on snow
or ice (Belopol'skii 1961)--presumably at increased incubation
costs. Lastly, certain species incubate eggs with their feet (e.g.,
cormorants), rather than develop featherless brood patches. There are
no measurements of comparative heat flow from feet versus brood patches.
Raising Nestlings
The length of the nestling period (hatching until departure from the
nest) varies greatly among northern seabirds (Fig. 6). Nestling period
depends on the stage of growth at which the young leave the nest and
the rate at which they attain that stage. Growth rate in turn depends
largely on body size and developmental type.
The stage of growth attained when birds leave the nest varies
considerably (Fig. 9). Precocial eiders leave the nest within a day of
hatching, whereas altricial shags remain until completely grown. The
young of semiprecocial species, on the other hand, leave the nest at
all stages between these extremes. Larids normally remain at the nest
until 75-90% grown, but certain alcids leave much sooner--well before
the young can fly.
[Illustration: Fig. 9. Percentage of total growth completed in the
egg (shaded bar at left), at the nest site (open bar), and after
nest-leaving (shaded bar at right) in various northern seabirds. From
Belopol'skii (1961).]
Growth rate depends both on body size and developmental type (Fig.
10). The length of stay at the nest for precocial young is unaffected
by growth rate (which is typically very slow), since they leave soon
after hatching. The nestling period of semiprecocial and altricial
seabirds is, however, affected by the rate at which the young grow to
the nest-leaving stage. This depends mainly on body size (Fig. 10)
and to a certain degree on developmental type, as some semiprecocial
species grow rather slowly. Certain seabirds with clutches of one egg
grow particularly slowly (petrels, some alcids, sulids). Several other
alcids with single-egg clutches, however, grow at rates normal for
semiprecocial chicks (Fig. 10). Very slow growth may be related to
food stress (Lack 1968; Ricklefs 1968) or to reduction of reproductive
effort in the adults (discussed later). Contrary to Cody (1973), slow
growth in alcids does not correlate to the distance adults must commute
for food. (Cody tried to directly compare growth in birds of different
sizes.) Chicks in nocturnal species, however, tend to have slow growth
rates (Sealy 1973_b_).
[Illustration: =Fig. 10.= Growth rate as a function of body weight.
Growth rate ᵗ10-90 represents the number of days to grow from 10% to
90% of asymptotic weight (Ricklefs 1968). Data from Ricklefs (1968,
1973), E. H. Dunn (1973), and Sealy (1973_b_). Solid circles and
regression line, altricial birds; solid triangles, semiprecocial birds
except for seabirds with one-egg clutches; open circles, precocial
shorebirds; open triangles, precocial ducks, rails, and gallinaceous
birds; solid squares, alcids with one-egg clutches; and open squares,
northern petrels, gannet, and Manx shearwater _(Puffinus puffinus)_.]
Daily time budgets of adults raising nestlings also vary widely,
depending on the amount of brooding required, food requirements of the
young, and foraging costs (which differ in the breeding season from
those at other times of the year).
Nestlings have imperfect control of body temperature at hatching
(Fig. 11) and develop this capacity only gradually. Altricial birds
are hatched at a particularly undeveloped stage; e.g., double-crested
cormorants attain reasonable control of body temperature in moderate
ambient temperatures only after about 14 days (Fig. 11; Table 5).
Semiprecocial seabirds, which are more fully developed physically at
hatching, attain control of body temperature much sooner, in a matter
of several days, and precocial eiders can thermoregulate within a few
hours after hatching (Table 5).
Until the age of temperature control, nestlings must be brooded
almost constantly, and occasional brooding takes place for some time
afterward, especially in severe weather, in all species studied
(Tinbergen 1960; Belopol'skii 1961; Weaver 1970; Dunn 1976_a_,
1976_b_). Thermoregulatory capabilities in cold weather are better
in ducklings of species nesting at high latitudes than at lower ones
(Koskimies and Lahti 1964), and the same may be true of gull species
(Dawson et al. 1972). The cooling mechanisms of double-crested
cormorants are better than in the more northerly distributed pelagic
cormorant, _Phalacrocorax pelagicus_ (Lasiewski and Snyder 1969). Thus,
variation in cost of thermoregulation due to different environments may
be reduced through adaptation.
Food requirements of the chick depend on growth rate, amount of fat
deposition, cost of thermoregulation, degree of activity and other
factors (E. H. Dunn 1973). Estimated energy budgets for nestling
double-crested cormorants and herring gulls in the same year and
locality (Fig. 12) indicate that these factors vary according to
developmental type, and comparison with budgets for nonseabird species
suggests wide variation within developmental types according to the
particular adaptations of each species to its own environment (E. H.
Dunn 1973).
[Illustration: Fig. 11. Development of thermoregulatory capabilities in
nestling double-crested cormorants. From Dunn (1976_a_). Ages at right
refer also to corresponding oxygen consumption data on the left. Thin
diagonal lines show equality between body and air temperature. All data
taken after 2 h of exposure.]
Thus, the energy demands of nestlings are not easy to predict. Brood
size differences multiply variation in food demand on adults (except
in precocial birds whose young feed themselves). Energy demands
are labile, however, particularly in requirements for activity and
growth, and adults can frequently raise young successfully without
providing optimum amounts of food (Spaans 1971; Kadlec et al. 1969;
LeCroy and Collins 1972; Lemmetyinen 1972; Cody 1973; E. H. Dunn and
I. L. Brisbin, manuscript in preparation). Studies of double-crested
cormorants by Dunn (1975_b_) and pigeon guillemots _(Cepphus columba)_
by Koelink (1972) have suggested that each adult providing optimum
amounts of food to a normal-sized brood would have to approximately
double the amount of food gathered each day over the amount gathered by
nonbreeders. This relation does not imply, however, that the time and
energy allocation of the adults would be the same for the two species.
[Illustration: Fig. 12. Energy budgets of nestling double-crested
cormorants and herring gulls. Data from E. H. Dunn (1973) and Brisbin
(1965).]
Cost-benefit ratios of food gathering in the nestling period differ
from those at other times. Besides facing increased food demands,
costs of delivery to the nest, and changes in food availability, the
parents' choice of foods is constrained by the need to forage within
reasonable commuting distance of the nest and perhaps by concentrated
competition with conspecifics and other seabird species. In addition,
small nestlings are frequently unable to eat foods normally eaten
by adults (Drent 1965; personal observation). In the face of these
constraints, adults often shift food preferences while raising
nestlings (Belopol'skii 1961). For example, female mew gulls in the
Barents Sea forage in the tidal zone, eating more small invertebrates
than at other times of the year, while males continue to forage at sea
and consume larger quantities of fish (Fig. 13).
Table 5. _Age of thermoregulatory control in various species of
northern seabirds._
Species Age when Source
moderate
temperature
control is
attained
(days)
Common eider 0.1-0.3[41] V. V. Rolnik, in Belopol'skii
(1961)
Herring gull 1.5-2 V. V. Rolnik, in Belopol'skii
(1961)
2-3 E. H. Dunn (1976_b_)
Leach's storm-petrel [2] Ricklefs (1974)
Mew gull 2-3 V. V. Rolnik, in Belopol'skii
(1961)
Lesser black-backed gull 2-3 E. K. Barth (in Farner and
Serventy 1959)
Greater black-backed gull 2-3 E. K. Barth (in Farner and
Serventy 1959)
Pigeon guillemot 2-4 Drent (1965)
Common tern 3 LeCroy and Collins (1972)
Roseate tern _(Sterna 3 LeCroy and Collins (1972)
dougallii)_
Common murre 3 V. V. Rolnik and Yu. M.
Kaftonowski (in Sealy 1973_b_)
Razorbill _(Alca torda)_ 3 V. V. Rolnik and Yu. M.
Kaftonowski (in Sealy 1973_b_)
Black guillemot 3-4 V. V. Rolnik, in Belopol'skii
(1961)
Tufted puffin 3.5[42] Cody (1973)
Northern phalarope 4-5[43] Hilden and Vuolanto (1972)
Cassin's auklet 5-6 Manuwal (1974_a_)
Horned puffin _(Fratercula 2-6 Sealy (1973_a_)
corniculata)_
Common puffin 6-7 V. V. Rolnik and Yu. M.
Kaftonowski (in Sealy 1973_b_)
Black-legged kittiwake 6-7 V. V. Rolnik, in Belopol'skii
(1961)
Double-crested cormorant 14 Dunn (1976_a_)
Shag 12-15 V. V. Rolnik, in Belopol'skii
(1961)
Commuting distances vary tremendously among species (Fig. 14), but
the number of feeding trips to the nest per day does not correlate
with foraging distance (Cody 1973; Sealy 1973_a_, 1973_b_). There
is not, therefore, a simple relationship between time and energy
expenditures of the adults and foraging distances. Nocturnality, on
the other hand, correlates with reduced feeding rates (usually one
visit to the nest each night). Seabirds feeding far from the colony
tend to show adaptations for bringing larger amounts of food per visit,
such as carrying more than one fish at a time, as in tufted puffins,
_Lunda cirrhata_, and rhinoceros auklets, _Cerorhinca monocerata_,
vs. guillemots and murres (Richardson 1961; Cody 1973; Sealy 1973_a_,
1973_b_); developing a sublingual storage pouch, as in Cassin's auklets
(Speich and Manuwal 1974); or concentration of food into stomach oil,
as in petrels and albatrosses (Ashmole 1971). Commuting costs are
largely eliminated when the young leave the nest, but only in the
alcids does nest leaving occur long before attainment of full growth.
Early nest leaving may allow adults and young to disperse to better
feeding areas than are exploitable from the colony site (Sealy 1973_b_)
and probably involves a major change in optimal food size and type as
well (Lind 1965).
Patterning of adult time budgets may differ between geographical
regions. For example, rhinoceros auklets are nocturnal in the far north
(where the summer night is particularly short), crepuscular in the
Olympic Peninsula, and mainly diurnal in the Farallon Islands (Manuwal
1974_a_).
[Illustration: Fig. 13. Foraging ranges of a pair of mew gulls during
the breeding season, on a Barents Sea colony. From Belopol'skii (1961).]
Food demands of nestlings have a great influence on the time and energy
allocation of breeding over nonbreeding seabirds. Because food is
particularly abundant in the reproductive season, however, one cannot
ascertain whether the vulnerability of breeding birds to time or energy
crises is far different from that at other times of the year.
Post-fledging Care
Little is known about the amount of care provided by adults to young
after they are fully grown. At least some species, such as gannets and
procellariiformes (Ashmole 1971), are known to desert their young,
whereas others are known to feed their young, at least occasionally,
for some weeks or months after they can fly--e.g., terns and gulls,
many alcids, and shags (Snow 1963; Vermeer 1963; Drury and Smith 1968;
Ashmole and Tovar S. 1968; Potts 1968; Ashmole 1971; LeCroy 1972).
[Illustration: Fig. 14. Percentage observations of foraging seabirds
at different distances from the nest site. After Cody (1973). Each
vertical bar represents 5% of total observations. Note nonlinear
horizontal scale.]
Annual Time and Energy Budgets
The discussion of time and energy allocation during reproduction was
complex and detailed because so much more is known about the influences
altering budgeting during this period than during other times of the
year. It is likely that influences on molt and migration will prove to
be equally complicated, once more is learned about them.
If all data on time and energy allocation for a single species were
known, it would be possible to make up detailed budgets for birds
of different age, sex, and experience throughout the year. However,
such detailed data have not been collected for any species. An annual
time budget for male and female yellow-billed magpie, _Pica nuttalli_
(Verbeek 1972), points out the great amount of difference between
the sexes (Fig. 15). A time and energy budget for the reproductive
season only (Fig. 16) shows large differences between two closely
related species, as well as between sexes; it also indicates the wide
difference between the budgeting of energy as opposed to budgeting of
time. All other time-energy budgets to date are for nonseabird species
and for only a portion of the annual cycle (Verbeek 1964; Verner 1965;
Schartz and Zimmerman 1971; Stiles 1971; Wolf and Hainsworth 1971;
Smith 1973; Utter and LeFebvre 1973).
[Illustration: Fig. 15. Time budget of male (upper panel) and female
(lower panel) yellow-billed magpies throughout the year. From Verbeek
(1972). Non-labeled portions in each graph correspond to labeled
sections in the other.]
Time-energy budget analysis can be useful in determining the leeway
a bird has in surviving unusual stress at different times of the
year. For example, a study by Feare et al. (1974) showed that rooks
_(Corvus frugilegus)_ in the dry part of the summer spent 90% of 15 h
of daylight to collect 150 kcal of food energy. In winter, foraging in
snow, the same birds were able to collect 240 kcal of food in only 30%
of a 10-h day. This suggests that rooks would be far more vulnerable
to unexpected periods of stress in late summer than in winter. Such
information would clearly be useful in making management decisions.
A more precise measure of vulnerability, although much more difficult
to determine, is that of productive energy--the amount of caloric
intake left over after the birds' cost of living (metabolic functions
and procurement and processing of food) have been accounted for. Costs
are highest when temperatures are extremely hot or cold or when food
is most difficult to obtain. Productive energy is highest in summer
(Kendeigh 1972), and that is presumably why reproduction normally takes
place then. It is unknown whether birds are more vulnerable to time and
energy shortages in the harder nonbreeding season or in the breeding
season after the extra demands of reproduction have been accounted for.
Vulnerability may also differ between sexes and among age groups.
Time-energy studies, although useful in comparing ecology, determining
vulnerability, and cataloging location of birds, do have limitations.
Careful studies are time-consuming and are not the best approach to
determining key factors influencing population increase or decrease.
Even when different kinds of data are being sought, however, it is
worthwhile keeping the time-energy framework in mind as a "big picture"
into which other facts can be fitted and their significance considered.
Life History Strategies
The study of life history strategies is largely theoretical, and in the
following discussion I do not comment on current theoretical arguments.
On the other hand, life history strategies can be regarded as time and
energy allocation on a grand scale, and it therefore seems appropriate
to look briefly at their implications for seabird management.
Annual reproduction evidently has a negative effect on resources
remaining for other functions, and may reduce the chances for an
organism to reproduce again in a later season (Cody 1966, 1971;
Williams 1966; Gadgil and Bossert 1970; Gadgil and Solbrig 1972;
Hussell 1972; Trivers 1972; Calow 1973). If the chances of survival
to another breeding season are small, the selective advantage lies
with the bird putting the most effort into early reproduction, in
spite of its negative effects on survival, because future chances of
reproduction are small. If chances of survival are good, however,
it may be more advantageous to reduce annual reproductive effort and
allocate resources to other functions.
[Illustration: Fig. 16. Time and energy budgets of male and female
red-winged _(Agelaius phoeniceus)_ and tricolored _(A. tricolor)_
blackbirds in the breeding season. From Orians (1961). Dotted lines
show male (M) activity, dashed lines show female (F) activity, and
solid lines show shared activities.]
Seabirds are generally long-lived, have small clutches, and generally
delay first breeding until at least the 2nd year, and usually longer
(Table 6). Phalaropes seem to differ from this pattern (Hilden and
Vuolanto 1972; Howe 1975). Several ecological factors (not entirely
independent) are believed to contribute to the evolution of the long
life and low reproductive effort pattern favored by seabirds.
First, if population size is determined largely by density-dependent
mortality, individuals may be favored that allocate resources to
attaining longer life (and more chances to reproduce) or insuring
greater chances of survival of their offspring (Murphy 1968; Hairston
et al. 1970). Density-independent mortality, on the other hand, is so
unpredictable that there is no advantage in allocating resources toward
protection against it (Gadgil and Solbrig 1972).
Two factors closely linked with density-dependence are high levels of
competition, and perennial difficulties in obtaining food. In adapting
to these difficulties, a bird may be selected which develops more
efficient foraging techniques, wider dispersal, or better abilities to
defend nesting territory--all of which may reduce resources available
for reproduction. As mentioned earlier, marine foods tend to be
patchily distributed, and a long learning period seems to be necessary
before seabirds become proficient at foraging. In addition, there is
evidence that food availability is low, at least in the tropics, and
perhaps in the winter in other regions (Ashmole 1971). If nesting
places are in short supply, long life may be favored so that the bird
can live long enough for a place to become vacant. Several authors
feel that competition is a serious factor in the life of seabirds,
both for food (Lack 1966; Cody 1973) and for nesting space (Snow 1960;
Belopol'skii 1961; Lack 1966; Manuwal 1974_b_). Others, however,
disagree, at least for the breeding season (e.g., Pearson 1968).
Table 6. _Life history data for certain northern seabirds._[44]
Annual adult Age at first
survival breeding Clutch
Species (%) (years) size
Fulmar 94 7+ 1
Gannet _(Morus bassanus)_ 94 (4)-5+ 1
Manx shearwater 93-96 (4)-5+ 1
Shag 85 (♂) (2)-3 3-4
80 (♀)
Herring gull 91-96 3.5 (♂) (2)-3
5 (♀)
Black-legged kittiwake 88 4-5 (♂) 3
3-4 (♀)
Arctic tern 89-91 (2)-3+ 2
75
82[45]
Common murre 87 3+? 1
Black guillemot 88+[46] 3?[46] 2[46]
Cassin's auklet 83[47] 3[47] 1
There is some evidence of density-dependent population size control in
seabirds, although much of it is circumstantial. For example, there
are large nonbreeding populations in such diverse species as shags,
herring gulls, and Cassin's auklets, which move into a breeding area
when established adults are removed or colonize new breeding areas
(J. C. Coulson, personal communication; Kadlec and Drury 1968; Drury
and Nisbet 1972; Manuwal 1974_b_). Lack (1966) and Ashmole (1971)
presented other arguments for density-dependence. Density-dependent
mortality is difficult to demonstrate, at best, and may be obscured by
interpopulation movements (Drury and Nisbet 1972).
If long life is a life history option, a low annual reproductive
effort could be favored in several ways. First, it may be necessary
for insuring long life, if breeding has a serious negative feedback on
life expectancy (Calow 1973). Second, if survival of offspring is more
unpredictable than that of adults, low annual effort may be selected
so that reproductive effort will not be wasted in years when young
have poor chances of survival. Unpredictable and variable first-year
survival in seabirds has been documented (Potts 1968; Drury and Nisbet
1972). In addition, some seabirds show adaptations that allow high
reproductive success in any given year but which do not drain off
resources if the season turns out to be poor (e.g., small last eggs in
the clutch or asynchronous hatching, both of which lead to elimination
of the smallest chicks when conditions are poor [Parsons 1970; E. H.
Dunn 1973]).
It should be emphasized that the factors involved in the evolution of
life histories are complex and poorly understood, and simple formulas
should not be expected to apply to all situations (Wilbur et al. 1974).
In the framework of life-history strategies, small clutch sizes and
slow growth rates exhibited by some seabirds can be explained as
adaptive reductions in annual reproductive effort, rather than as
responses to immediate food shortages. Arguments for this view are
presented on theoretical grounds (Dunn 1973) and by the fact that
many seabirds are able to raise larger than normal broods in certain
situations (Vermeer 1963; Nelson 1964; Harris 1970; Hussell 1972;
Ward 1972; Corkhill 1973). In addition, seabirds with particularly
slow growth rates all grow at about the same rate, regardless of body
size (contrary to the situation in other birds). This suggests that
low growth rates do not reflect variations in feeding abilities among
species (Ricklefs 1968).
Several conclusions relating to management of seabird populations
can be drawn from the above discussion. First, if population size is
determined largely by density-dependent factors, the birds are not
adapted to precipitous and unexpected declines in population levels.
Because there is low annual reproductive effort geared to a world in
which there is slow turnover in population, seabirds are not able to
rebound quickly from disasters. Provision of excess food should not be
expected to improve breeding performance, at least in experienced birds.
Second, because seabirds are able to reproduce in many different
seasons and are adapted to a low reproductive effort within a given
season, one should expect them to be easily disturbed and to fail to
complete the reproductive cycle during any given breeding attempt. A
few indications of such failures have already been observed (Erskine
1972; Manuwal 1974_a_; Nettleship 1975).
Again, the tentative nature of this discussion should be emphasized,
and conclusions drawn from it may not apply equally to all seabird
species.
Conclusions
In this discussion I have tried to emphasize the variety of factors
affecting seabird life cycles and the diverse responses among different
species to their environment. The main conclusion I stress is that each
species (and age group and sex within that species) has a different
vulnerability to stress, which may be most severe at different times
of the year for each group. To determine these periods of stress,
researchers may find a time-energy approach to be useful.
As for northwestern North American seabirds in particular, ignorance is
vast. Twelve years ago, Bourne (1963:846) noted the following needs in
seabird research (among others): "The investigation of seabird biology
has been reduced to a routine, but there is a great need for more study
of some other aspects of the life or annual cycle, including events in
the period immediately after fledging, and behaviour and survival in
the immature period and outside the breeding season. Much more accurate
information is needed about breeding distribution and seasons in many
parts of the world, about molting seasons and ranges in most parts, and
the distribution of birds of different age groups during these periods
in practically all areas."
Since the time of Bourne's remarks, a number of excellent studies have
provided data on the breeding biology of certain northwestern seabird
species. Scientists remain largely ignorant, however, about where birds
of different age groups are located throughout the year. Such knowledge
is necessary for effective protection and is basic to understanding
population dynamics, even if it does not elucidate causes. Studies
of timing of annual cycles and movements should be carried out hand
in hand with resource analysis--not just finding what birds eat, but
discovering where the food is at what times, how hard it is to catch,
and what the nutritional return is. Much careful field work must be
done before effective management of most of our northwestern seabirds
can become a reality.
References
Andersson, M. 1973. Behaviour of the pomarine skua _Stercorarius
pomarinus_ Temm. with comparative remarks on Stercorariinae.
Ornis Scand. 4:1-16.
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.
Ashmole, N. P., and H. Tovar S. 1968. Prolonged parental care in
royal terns and other birds. Auk 85:90-100.
Barash, D. P., P. Donovan, and R. Myrick. 1975. Clam dropping
behavior of the glaucous-winged gull _(Larus glaucescens)_.
Wilson Bull. 87:60-64.
Bateson, P. P. G., and R. C. Plowright. 1959. The breeding biology
of the ivory gull in Spitsbergen. Br. Birds 52:105-114.
Bédard, J. 1969_a_. Feeding of the least, crested and parakeet
auklets around St. Lawrence Island, Alaska. Can. J. Zool.
47:1025-1050.
Bédard, J. 1969_b_. Adaptive radiation in alcidae. Ibis 111:189-198.
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.
Bengtson, S. 1968. Breeding behavior of the grey phalarope in west
Spitzbergen. Var Fågelvärld 27:1-13.
Berger, M., and J. S. Hart. 1974. Physiology and energetics of
flight. Pages 415-477 _in_ D. S. Farner and J. R. King, eds.
Avian biology. Vol. IV. Academic Press, New York.
Berger, M., J. S. Hart, and O. Z. Roy. 1970. Respiration, oxygen
consumption and heart rate in some birds during rest and flight.
Z. Vgl. Physiol. 66:201-214.
Birkhead, T. R. 1974. Movement and mortality rates of British
guillemots. Bird Study 21:241-254.
Blackmore, F. H., Jr. 1969. The effect of the temperature,
photoperiod and molt on the energy requirements of the house
sparrow, _Passer domesticus_. Comp. Biochem. Physiol. 30:433-444.
Bookhout, T. A. 1958. The availability of plant seeds to bobwhite
quail in southern Illinois. Ecology 39:671-681.
Bourne, W. R. P. 1963. A review of oceanic studies of the biology
of seabirds. Proc. Int. Ornithol. Congr. 13:831-854.
Brisbin, I. L., Jr. 1965. A quantitative analysis of ecological
growth efficiency in the herring gull. M.S. Thesis. Univ. of
Georgia, Athens. 28 pp.
Brown, R. G. B., N. G. Blurton-Jones, and D. J. T. Hussell. 1967.
The breeding behaviour of Sabine's gull, _Xema sabini_. Behaviour
28:110-140.
Bryant, D. M. 1973. The factors influencing the selection of food
by the house martin (_Delichon urbica_ (L.)). J. Anim. Ecol.
42:539-564.
Buckley, F. G., and P. A. Buckley. 1974. Comparative feeding
ecology of wintering adult and juvenile royal terns (Aves:
Laridae, Sterninae). Ecology 55:1053-1063.
Calder, W. A. 1974. Consequences of body size for avian energetics.
Pages 86-144 _in_ R. A. Paynter, ed. Avian energetics. Publ.
Nuttall Ornithol. Club 15.
Calder, W. A., and J. R. King. 1974. Thermal and caloric relations
of birds. Pages 259-413 _in_ D. S. Farner and J. R. King, eds.
Avian biology. Vol. IV. Academic Press, New York.
Calow, P. 1973. The relationship between fecundity, phenology, and
longevity: a systems approach. Am. Nat. 107:559-574.
Cody, M. L. 1966. A general theory of clutch size. Evolution
20:174-184.
Cody, M. L. 1971. Ecological aspects of reproduction. Pages 461-512
_in_ D. S. Farner and J. R. King, eds. Avian biology. Vol. I.
Academic Press, New York.
Cody, M. L. 1973. Coexistence, coevolution and convergent evolution
in seabird communities. Ecology 54:31-44.
Cohen, D. 1967. Optimization of seasonal migratory behavior. Am.
Nat. 101:5-17.
Cone, C. D., Jr. 1964. A mathematical analysis of the dynamic
soaring flight of the albatross with ecological interpretations.
Va. Inst. Mar. Sci., Spec. Sci. Rep. 50:1-104.
Corkhill, P. 1973. Food and feeding ecology of puffins. Bird Study
20:207-220.
Coulson, J. C. 1961. Movements and seasonal variation in
mortality of shags and cormorants ringed on the Farne Islands,
Northumberland. Br. Birds 54:225-235.
Coulson, J. C. 1963. Egg size and shape in the kittiwake _(Rissa
tridactyla)_ and their use in estimating age composition in
populations. Proc. Zool. Soc. Lond. 140(2):211-227.
Coulson, J. C., and M. G. Brazendale. 1968. Movements of cormorants
ringed in the British Isles and evidence of colony-specific
dispersal. Br. Birds 61:1-21.
Coulson, J. C., G. R. Potts, and J. Horobin. 1969. Variation in the
eggs of the shag _(Phalacrocorax aristotelis)_. Auk 86:232-245.
Coulson, J. C., and E. White. 1958. The effect of age on the
breeding biology of the kittiwake, _Rissa tridactyla_. Ibis
100:40-51.
Coulson, J. C., and E. White. 1960. The effect of age and density
of breeding birds on the time of breeding of the kittiwake,
_Rissa tridactyla_. Ibis 102:71-80.
Cox, G. W. 1968. The role of competition in the evolution of
migration. Evolution 22:180-192.
Cramp, S. 1972. The breeding of urban wood pigeons. Ibis
114:163-171.
Cullen, J. M. 1957. Plumage, age and mortality in the arctic tern.
Bird Study 4:197-207.
Dawson, W. R., and J. W. Hudson. 1970. Birds. Pages 223-310 _in_ G.
C. Whittow, ed. Comparative physiology of thermoregulation. Vol.
I. Academic Press, New York.
Dawson, W. R., J. W. Hudson, and R. W. Hill. 1972. Temperature
regulation in newly hatched laughing gulls _(Larus atricilla)_.
Condor 74:177-184.
Dolnik, V. R. 1971. Comparative energy expenditure in migration and
wintering birds. Ekologiya 2(3):88-89. In Russian.
Dorst, J. 1961. The migrations of birds. William Heinimann Ltd.,
London.
Drent, R. H. 1965. Breeding biology of the pigeon guillemot
_Cepphus columba_. Ardea 53:99-160.
Drent, R. H. 1970. Functional aspects of incubation in the herring
gull (_Larus argentatus_ Pont.). Behaviour Suppl. 17:1-132.
Drent, R. 1972. Adaptive aspects of the physiology of incubation.
Proc. Int. Ornithol. Congr. 15:255-280.
Drent, R. H., and C. J. Guiguet. 1961. A catalogue of British
Columbia seabird colonies. B. C. Prov. Mus., Occas. Pap. 12:1-173.
Drent, R., G. F. van Tets, F. Tompa, and K. Vermeer. 1964. The
breeding birds of Mandarte Island, British Columbia. Can.
Field-Nat. 78:208-263.
Drury, W. H., and I. C. T. Nisbet. 1972. The importance of
movements in the biology of herring gulls in New England. Pages
173-212 _in_ Population ecology of migratory birds: a symposium.
U.S. Fish Wildl. Serv., Wildl. Res. Rep. 2.
Drury, W. H., Jr., and W. J. Smith. 1968. Defense of feeding
areas by adult herring gulls and intrusion by young. Evolution
22:193-201.
Dunn, E. H. 1973. Energy allocation of nestling double-crested
cormorants. Ph.D. Thesis. Univ. of Michigan, Ann Arbor. 153 pp.
Dunn, E. H. 1975_a_. Growth, body components and caloric value of
nestling double-crested cormorants. Condor 77:431-438.
Dunn, E. H. 1975_b_. Caloric intake of nestling double-crested
cormorants. Auk 92:553-565.
Dunn, E. H. 1976_a_. Development of endothermy and existence
energy expenditure of nestling double-crested cormorants. Condor
78:350-356.
Dunn, E. H. 1976_b_. Development of endothermy and existence energy
expenditure in herring gull chicks. Condor 78:493-498.
Dunn, E. K. 1972. Effect of age on the fishing ability of sandwich
terns _Sterna sandvicensis_. Ibis 114:360-366.
Dunn, E. K. 1973. Changes in fishing ability of terns associated
with wind speed and sea surface conditions. Nature (Lond.)
244:520-521.
Eliassen, E. 1963. Preliminary results from new methods of
investigating the physiology of birds during flight. Ibis
105:234-237.
Emlen, J. M. 1966. The role of time and energy in food preference.
Am. Nat. 100:611-617.
Erskine, A. J. 1972. The great cormorants of eastern Canada. Can.
Wildl. Serv. Occas. Pap. 14:1-23.
Evans, R. M., and M. K. McNicholl. 1972. Variations in reproductive
activities of arctic terns at Churchill, Manitoba. Arctic
25:131-141.
Farner, D. S., and D. L. Serventy. 1959. Body temperature and the
ontogeny of thermoregulation in the slender-billed shearwater.
Condor 61:426-433.
Feare, C. J., G. M. Dunnet, and I. J. Patterson. 1974. Ecological
studies of the rook (_Corvus frugilegus_ L.) in north-east
Scotland: food intake and feeding behaviour. J. Appl. Ecol.
11:867-896.
Fisher, H. 1972. The nutrition of birds. Pages 431-469 _in_ D. S.
Farner and J. R. King, eds. Avian biology. Vol. II. Academic
Press, New York.
Fisher, R. A. 1958. The genetical theory of natural selection. 2nd
rev. ed. Dover Publishers, Inc., New York.
Gadgil, M., and W. H. Bossert. 1970. Life historical consequences
of natural selection. Am. Nat. 104:1-24.
Gadgil, M., and O. T. Solbrig. 1972. The concept of r-and
K-selection: evidence from wild flowers and some theoretical
considerations. Am. Nat. 106:14-31.
Gavrilov, V. 1974. Metabolism of molting birds. Zool. Zh.
53(9):1363-1374. In Russian, English summary.
Gross, A. O. 1935. The life history cycle of Leach's petrel
_(Oceanodroma leucorhoa leucorhoa)_ on the outer sea islands of
the Bay of Fundy. Auk 52:382-399.
Hainsworth, F. R., and L. L. Wolf. 1975. Wing disc loading:
implications and importance for hummingbird energetics. Am. Nat.
109:229-233.
Hairston, N. G., D. W. Tinkle, and H. M. Wilbur. 1970. Natural
selection and the parameters of population growth. J. Wildl.
Manage. 34:681-690.
Harris, M. P. 1970. Breeding ecology of the swallow-tailed gull,
_Creagus furcatus_. Auk 87:215-243.
Harris, M. P. 1971. Ecological adaptations of moult in some British
gulls. Bird Study 18:113-118.
Harris, S. W. 1974. Status, chronology, and ecology of nesting
storm petrels in northwestern California. Condor 76:249-261.
Hart, J. S., and M. Berger. 1972. Energetics, water economy and
temperature regulation during flight. Proc. Int. Ornithol. Congr.
15:189-199.
Henderson, B. A. 1972. The control and organization of parental
feeding and its relationships to the food supply for the
glaucous-winged gull, _Larus glaucescens_. M.S. Thesis. Univ. of
British Columbia, Vancouver.
Hilden, O., and S. Vuolanto. 1972. Breeding biology of the
red-necked phalarope _Phalaropus lobatus_ in Finland. Ornis Fenn.
49:57-81.
Högstedt, G. 1974. Length of the pre-laying period in the lapwing
_Vanellus vanellus_ L. in relation to its food resources. Ornis
Scand. 5:1-4.
Höhn, E. O. 1971. Observation on the breeding behavior of grey and
red-necked phalaropes. Ibis 113:335-348.
Howe, M. A. 1975. Behavioral aspects of the pair bond in Wilson's
phalarope. Wilson Bull. 87:248-270.
Hunt, G. L., Jr. 1972. Influence of food distribution and human
disturbance on the reproductive success of herring gulls. Ecology
53:1051-1061.
Hussell, D. J. T. 1969. Weight loss of birds during nocturnal
migration. Auk 86:75-83.
Hussell, D. J. T. 1972. Factors affecting clutch size in arctic
passerines. Ecol. Monogr. 42:317-364.
Ingolfsson, A. 1969. Behaviour of gulls robbing eiders. Bird Study
16:45-52.
Ingolfsson, A. 1970. The moult of remiges and rectrices in great
black-backed gulls _Larus marinus_ and glaucous gulls _L.
hyperboreus_ in Iceland. Ibis 112:83-92.
James-Veitch, E., and E. S. Booth. 1974. Behavior and life history
of the glaucous-winged gull. Walla Walla Coll. Publ. 12:1-39.
Johnston, D. W. 1961. Timing of annual molt in the glaucous gulls
of northern Alaska. Condor 63:474-478.
Kadlec, J. A., and W. H. Drury. 1968. Structure of the New England
herring gull population. Ecology 49:644-676.
Kadlec, J. A., W. H. Drury, Jr., and D. K. Onion. 1969. Growth and
mortality of herring gull chicks. Bird-Banding 40:222-233.
Källender, H. 1974. Advancement of laying of great tits by the
provision of food. Ibis 116:365-367.
Katz, P. L. 1974. A long-term approach to foraging optimization.
Am. Nat. 108:758-782.
Kendeigh, S. C. 1970. Energy requirements for existence in relation
to size of bird. Condor 72:60-65.
Kendeigh, S. C. 1972. Monthly variations in the energy budget of
the house sparrow throughout the year. Pages 17-43 _in_ S. C.
Kendeigh and J. Pinowski, eds. Productivity, population dynamics
and systematics of granivorous birds. Institute of Ecology,
Polish Academy of Science, Warsaw.
Kendeigh, S. C. 1973. [Discussion.] Pages 311-320 _in_ D. S.
Farner, ed. Breeding biology of birds. National Academy of
Sciences, Washington, D.C.
King, J. R. 1973. Energetics of reproduction in birds. Pages 78-107
_in_ D. S. Farner, ed. Breeding biology of birds. National
Academy of Science, Washington, D.C.
King, J. R. 1974. Seasonal allocation of time and energy resources
in birds. Pages 4-70 _in_ R. A. Paynter, ed. Avian energetics.
Publ. Nuttall Ornithol. Club 15.
Koelink, A. F. 1972. Bioenergetics of growth in the pigeon
guillemot, _Cepphus columba_. M.S. Thesis. Univ. of British
Columbia, Vancouver.
Koskimies, J., and L. Lahti. 1964. Cold-hardiness of the newly
hatched young in relation to ecology and distribution in ten
species of European ducks. Auk 81:281-307.
Lack, D. 1966. Population studies of birds. Clarendon Press, Oxford.
Lack, D. 1968. Ecological adaptations for breeding in birds.
Methuen, London.
Lasiewski, R. C. 1963. Oxygen consumption of torpid, resting,
active and flying hummingbirds. Physiol. Zool. 36:122-140.
Lasiewski, R. C., and W. R. Dawson. 1967. A reexamination of the
relation between standard metabolic rate and body weight in
birds. Condor 69:13-23.
Lasiewski, R. C., and G. K. Snyder. 1969. Responses to high
temperature in nestling double-crested cormorants and pelagic
cormorants. Auk 86:529-540.
LeCroy, M. 1972. Young common and roseate terns learning to fish.
Wilson Bull. 84:201-202.
LeCroy, M., and C. T. Collins. 1972. Growth and survival of roseate
and common tern chicks. Auk 89:595-611.
Lemmetyinen, R. 1972. Growth and mortality in the chicks of arctic
terns in the Kongsfjord area, Spitzbergen in 1970. Ornis Fenn.
49:45-53.
Lind, H. 1965. Parental feeding in the oystercatcher _Haematopus o.
ostralegus_ (L.). Dan. Ornithol. Foren. Tidsskr. 59:1-31.
Lustick, S. 1970. Energy requirements of molt in cowbirds. Auk
87:742-746.
Manuwal, D. A. 1974_a_. The natural history of Cassin's auklet
_(Ptychoramphus aleuticus)_. Condor 76:421-431.
Manuwal, D. A. 1974_b_. Effects of territoriality on breeding in a
population of Cassin's auklet. Ecology 55:1399-1406.
Martin, E. W. 1968. The effects of dietary protein on the energy
and nitrogen balance of the tree sparrow _(Spizella a. arborea)_.
Physiol. Zool. 41:313-331.
McKinney, F. 1961. An analysis of the displays of the European
eider _Somateria mollissima mollissima_ (Linnaeus) and the
Pacific eider _Somateria mollissima v. nigra_ Bonaparte.
Behaviour Suppl. 7:1-124.
Moss, R. 1972. Food selection by red grouse (_Logopus logopus
scoticus_ (Lath.)) in relation to chemical composition. J. Anim.
Ecol. 4:411-428.
Moyle, P. 1966. Feeding behavior of the glaucous-winged gull on the
Alaskan salmon stream. Wilson Bull. 78:175-190.
Murphy, G. I. 1968. Patterns in life history and the environment.
Am. Nat. 102:391-403.
Myrberget, S. 1962. Contribution to the breeding biology of the
puffin _Fratercula arctica_ (L.). Eggs, incubation and young.
Pap. Norw. State Game Res. Inst. Ser. 2, 11:1-49.
Myton, B. A., and R. W. Ficken. 1967. Seed size preference in
chickadees and tits in relation to ambient temperatures. Wilson
Bull. 79:319-321.
Nelson, J. B. 1964. Factors influencing clutch-size and chick
growth in the North Atlantic gannet _Sula bassana_. Ibis
106:63-77.
Nettleship, D. N. 1972. Breeding success of the common puffin
(_Fratercula arctica_ L.) on different habitats at Great Island,
Newfoundland. Ecol. Monogr. 42:239-268.
Nettleship, D. N. 1975. A recent decline of gannets, _Morus
bassanus_, on Bonaventure Island, Quebec. Can. Field-Nat.
89:125-133.
Nice, M. M. 1962. Development of behavior in precocial birds.
Trans. Linn. Soc. N. Y. 8:1-211.
Nisbet, I. C. T. 1963. Weight-loss during migration. 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.