Conservation of marine birds of northern North America: / papers from the international symposium held at the Seattle Hyatt House

by Unknown

Population Dynamics in Northern Marine Birds

by

William H. Drury

College of the Atlantic
Bar Harbor, Maine 04609

Abstract

It seems only reasonable to assume that populations of marine birds fluctuate even when not disturbed by man; such fluctuations would result both from the secondary effects of species adaptive tactics and from changes in the marine environment. I briefly review some human activities and some other natural processes that have resulted in changes in numbers and distribution of seabirds and present a short discussion of theoretical models which emphasizes that conclusions drawn or predictions made from models of the dynamics of populations depend upon the assumptions about stability that were used in preparing the models. I then review those special characteristics of seabirds which are directly relevant to planning programs intended to protect seabirds or encourage their increase and identify several goals for improving our understanding of the population dynamics and biology of marine birds. My general conclusion is that enough is already known to undertake effective conservation programs, and that time is pressing.

Seabirds have been categorized as renewable resources in only a few places, although their symbolic value has been recognized for centuries (for example, the medieval poem "The Seafarer" and the designs on Saint Cuthbert's tunic). With the exception of the Russians (Belopol'skii 1961; Uspenski 1956), the Australians (Serventy 1967), and the Icelanders, industrialized peoples have not considered seabirds to be salable and therefore worth managing. Yet during many centuries the seabirds of the northern seas were a major food for coastal and island villages (Bent 1919, 1921, 1922; Fisher and Lockley 1954).

Some biological principles that affect the dynamics of seabird populations are identified in this paper. I believe these principles must form the basis of plans to maintain and increase seabird numbers.

I describe some observations of population changes, review briefly the conflicting theoretical frameworks for population dynamics, and identify some of the biological characteristics of marine birds that affect the way in which population changes occur. The terms "seabirds" and "marine birds" are used interchangeably for those bird species which depend upon salt water for some part of their annual cycle (c.f., the Pacific Seabird Group).

Population Fluctuations

Broadly stated, the populations of northern seabirds have shown marked short-and long-term fluctuations. Most authors have assumed that all such fluctuations reflect human disturbance of the natural system, because of the obvious effects of human predation during the last 200 years.

Human Impact

In the centuries before people traveled extensively between islands, seabirds were taken in ways that we judge must have allowed the survival of the colonies (e.g., those at the Faroes or Saint Kilda, those in Iceland and Greenland, or those in the Aleutian Islands and the Bering Strait). We presume either that the populations of island peoples were regulated by shortage of resources other than seabirds or that those who overcropped and eliminated the seabirds suffered the consequences.

Negative Effects

When a sea-going, commodity-oriented way of life evolved, seabirds were killed in huge numbers for such uses as the plumage trade, fish bait, or rendering into oil (Tuck 1960; Fisher and Lockley 1954). Even the elimination of several colonies—e.g., Funk Island, Newfoundland (Tuck 1960); Seal Island, Eastern Egg Rock, Maine (Norton 1921); Muskeget, Massachusetts (Forbush 1929)—may have had little effect on the rate of cropping because those who killed off one source could probably seek out another. As the colonial seabirds became scarce they became more valuable, which stimulated more intensive pursuit of the remnants (Dutcher 1901, 1904).

In some places where seabird colonies did not supply a croppable economic resource, the islands were used for alternative crops with at least temporary commodity value (e.g., foxes were introduced in the Aleutian Islands; Bent 1919). Large herbivores were introduced to supply meat for island residents (e.g., Saint Matthew Island; Klein 1959), as well as pigs, cattle, sheep, goats, and rabbits on islands in the North Atlantic and southern oceans (many authors). Increases in many seabird populations over the last 75 years have been generally associated with relief from predation by humans such as the fowlers, eggers, and plume hunters of the 19th century. Such relief may have been partly responsible for the increase of North Atlantic gannets, Sula bassana, and common murres or guillemots, Uria aalge (Fisher and Vevers 1943, 1944; Cramp et al. 1974). On a smaller scale, several population increases along the coast of New England have been recorded following the enactment of protective legislation (Dutcher 1901, 1904; Norton 1921, 1924; Palmer 1949; Drury 1973).

Coulson (1974) argued that in addition to relief from predation, the explosion of the population of kittiwakes (Rissa tridactyla) in this century resulted from access to previously un-occupiable breeding sites. Nesting cliffs and buildings suitable for kittiwake nesting are abundant and now protected from egging or fowling.

Positive Effects

There can be little doubt that human activities have also had marked positive effects in some cases. For example, Fisher (1952) suggested that the North Atlantic fulmar (Fulmarus glacialis) was provided food first by whaling, then by commercial fishing, and that this food allowed the species to increase steadily over the last 3 centuries.

The worldwide increase of gulls (Larus argentatus, L. fuscus, L. dominicanus, L. ridibundus, L. novae-hollandii) has been credited to availability of food from wasteful human garbage disposal (Murray and Carrick 1964; Fordham 1968, 1970; Harris 1964; Harris and Plumb 1965; Kadlec and Drury 1968; Brown 1967; Mills 1973; Vermeer 1963).

It is hard to dismiss the evidence pointing to the impact of human activities on seabird populations during the last 3 centuries. Yet it would be misleading to assume that without man's interference seabird populations would have remained stable. Success in designing programs of protection and population enhancement must allow for the realities—that seabird populations fluctuate inherently, and that secular changes occur regularly in their environment.

Impact of Natural Events

Some population changes appear to result from sudden impacts; other changes are gradual.

Sudden Disasters

Gromme (1927) reported windrows of dead murres in the Unimak Pass and Alaska Peninsula; die-offs of murres in winter storms in the Atlantic and Arctic Oceans were reported by Tuck (1960) and Dement'ev et al. (1968).

Recently some mass mortalities have been associated with specific causes. Bailey and Davenport (1972) reported that starvation caused the die-off of common murres in the southern Bering Sea—Bristol Bay area. Foul weather, which apparently inhibited feeding between 19 and 23 April 1970, culminated in an intense storm. Similarly in late winter 1969 bad weather in the Irish Sea, combined with strains of molt and perhaps contamination with industrial chemicals, seems to have contributed to mass mortality of the same species (called common guillemot in Britain; Holdgate 1971). The seabird victims of this event had metabolized their body fat and as a result, polychlorinated biphenyls (PCB) and other industrial chemicals passed into livers, kidneys, and brains. Again, a storm at the end of a period of stress seems to have been more than the birds could tolerate.

A further example of a die-off of waterfowl apparently brought on by starvation was given by Barry (1968), who estimated that about 100,000 king eiders (Somateria spectabilis) died when they arrived before the ice broke up in the Beaufort Sea in spring 1964.

Diseases have produced massive die-offs in marine birds. Fowl cholera caused high mortality in nesting common eiders (Somateria mollissima) in the Gulf of St. Lawrence in Quebec (Reed and Cousineau 1967) and in Penobscot Bay, Maine, in the early 1960's (H. Mendall, personal communication). Poisoning from a "red tide" (a bloom of the dinoflagellate Gonyaulax tamerensis) caused a die-off of black ducks (Anas rubripes) and herring gulls on the coast of New England in 1972. Similarly a die-off of shags (Phalacrocorax aristotelis) on the east coast of England was caused by a "red tide" (Coulson et al. 1968). During a period of 1 week 90% of the shag nests on the Farne Islands in Northumberland were deserted and about 80% of the breeding population died.

Gradual Declines

When the new volcanic island of Bogoslov emerged in the western Aleutians, Preble and McAtee (1923) reported that it was colonized by large numbers of pigeon guillemots (Cepphus columba), but in the following decades the guillemots have steadily decreased (G. J. Divoky, personal communication). As a further example, the nesting population of Atlantic puffins (Fratercula arctica) in the Atlantic has declined over the past several years, especially those nesting on the Outer Hebrides (Flegg 1972; Harris 1976).

It is difficult to find seabird species whose nesting grounds have not been affected by humans but whose numbers have been censused. The best illustrations of secular changes in relatively constant habitats are probably those available in the British Trust for Ornithology's breeding censuses of songbirds. Songbirds are short-lived and their populations change on relatively short time scales. The northwestern European landscape has remained relatively constant for the last 75 years, yet there are observable decade-long trends—for example, of willow warblers (Phylloscopus trochilus) and dunnock (Prunella modularis). There are detailed data on population changes in great tits (Parus major) through the work of Kluyver (1951), Lack (1964), and Perrins (1965).

Effects Reflecting Environmental Change

Nelson (1966) argued that the increase of gannets in the North Atlantic during this century has been related to increasing temperatures rather than (as usually ascribed) to increased food from fish damaged or escaped during commercial fishing.

Ainley and Lewis (1974) described a particularly interesting example of the effects of environmental change on seabird populations. The events begin with the decrease of seabirds on the Farallon Islands off California as a result of human depredations. Even after fowling was made illegal, the populations of murres, double-crested cormorants (Phalacrocorax auritus), and especially of tufted puffins (Lunda cirrhata) and pigeon guillemots continued to decline as a result of oil pollution. During the last 3 decades the smaller species of seabirds nesting on the Farallons, such as rhinoceros auklets (Cerorhinca monocerata), have increased rapidly and the authors suggest that their increase was abetted by an increase in the small prey fish, northern anchovy (Engraulis mordax). One of course expects predators to be affected by changes in the abundance of their prey. During this same period, larger species of seabirds such as double-crested cormorants and tufted puffins have failed to recover their numbers, and the authors speculate that this failure is related to a decrease of the larger prey fish, Pacific sardine (Sardinops caerulea).

A widely publicized impact of environmental fluctuation upon seabird populations is that of the northeast wind, El Niño, off the Peruvian coast. This wind pushes the upwelling Humboldt Current water offshore and causes mass mortality in the Peruvian anchovies (Engraulis ringens) and, as a consequence, a die-off among the millions of seabirds such as Peruvian guanay cormorants (Phalacrocorax bougainvillii) and Peruvian boobies or piquero (Sula variegata) which feed upon them (Murphy 1936).

Theoretical Considerations

Can useful generalizations be drawn from these observations on population changes? Can a model be constructed of the forces which drive population changes or of population-habitat interactions which keep populations from extinction? Some conflicting theories and assumptions of population dynamics are examined and discussed below.

The Assumption of Population Stability and of Closely Attuned Density-dependent Mortality

During the 5 decades before 1970, it was widely accepted that most animal populations were generally stable and saturated before the arrival of the white man. Although a few field biologists vigorously dissented, "establishment" ecologists regarded fluctuations as a departure from the norm, and as such, a hazard to the population. Many theorists of both evolution and ecology argued that adaptations were required to damp fluctuations or the fluctuations would become "random walks" and the population would rapidly become extinct. As a consequence, relatively all theoretical models included stability as a central assumption.

• The basic element of this theoretical complex has been the Lotka-Volterra formula for a logistic curve of population growth and stabilization. According to this formula it has been reasoned that by establishing the inherent rate of increase of a population (i.e., its average natality relative to mortality, or r) and by measuring the carrying capacity of the environment (which is the density of the population at saturation, or K), one can predict the maximally productive population size, and maximum rate of production of new individuals (or maximum sustained yield). These assumptions have supplied the theoretical framework for virtually all game management and many fisheries practices.

Once stability was assumed, a mechanism for maintaining stability was necessary. This mechanism was found in an interaction between the population and the environment, called density-dependent mortality (Nicholson 1933). The impact of this feedback has been assumed to cause the point of inflection of the "sigmoid curve" and to regulate the density "at equilibrium."

Populations growing in relatively isolated or closed systems have been observed to follow a sigmoid curve toward a steady state. We have data on the growth of several Massachusetts gull colonies which show this type of short-period rapid increase followed by a long sequence of shallow oscillations (Drury and Nisbet 1972). But usually observations have been terminated at about the time the population passed through the point of inflection.

• Lack (1954) accepted the principles formulated by Lotka-Volterra and hence viewed Nicholson's (1933) density-dependence as logically necessary. Lack (1948, 1954) argued that reproductive effort (clutch size or litter size times the number of broods) must be as large as the parents can successfully raise to independence because these biological characteristics are directly subject to natural selection. He argued that because reproductive potential is excessive (Darwin 1859), mortality must be density-dependent if a population is to avoid fluctuations. The only adequately density-dependent regulating process he accepted was the population's response to its food supply (Lack 1954). In fact, for many years Lack rejected Kluyver and Tinbergen's (1953) hypothesis that territory could act as a control on population size in birds because, he argued, territories were compressible and therefore allowed wide fluctuations. To his credit, however, Lack eventually acknowledged this mistake.

The first defect in the concept of "carrying capacity" is the idea that populations have "mechanisms" or "institutions" (Wynne-Edwards 1959) by which the population is kept stable at the carrying capacity in a stable habitat.

The second defect in the concept of carrying capacity is that it presupposes a stable environment. During the early decades of the 20th century most climatologists believed that a departure from the norms of a regional climate set processes in motion which would return the climate to normal. During the last decades, however, climatologists and oceanographers have shown clearly that environments are continuously in flux.

An Attack on Density-dependent Mortality

Some theorists rejected the concept of carrying capacity as soon as it was formulated. Andrewartha and Birch (1954) predicted fluctuations would be undamped by inherent population mechanisms but rather would be controlled by external forces indifferent to the density. Their supporting data were drawn from field studies of insects in arid climates. Some of their ideas are directly relevant to seabirds; for example, their assertion that in many cases limits to carrying capacity of the habitat are not set in a way responsive to the density of the population. The number of occupiable ledges on a seabird cliff are fixed and when they are full no more birds can breed there regardless of the amount of food available. For another example, some biological processes act in a way that reinforces fluctuations. Predation can act in this way in the relatively closed system of a seabird colony; i.e., the smaller the prey population the larger the percentage taken by the predators. The importance of predation as a selecting factor is shown by the adaptations marine birds and waterfowl make to avoid it. The fact that large colonies of seafowl are usually concentrated on isolated, predator-free islands is one obvious case (Lack 1966).

Although their ideas are useful in understanding changes in many species, primarily insect populations, the generality of Andrewartha and Birch's (1954) hypothesis is weakened because it conflicts with detailed studies of seabirds which show that in many cases local food resources do limit breeding success. Ashmole (1963) showed this for tropical terns, and Hunt (1972) for some colonies of herring gulls on the New England coast. Nettleship (1972), studying the effects of herring gulls on Atlantic puffins, showed that the effect of harassment and stealing food from the parents was to reduce the amount of food brought to the young and thus reproductive success. In those parts of the colony where gulls were numerous or where the puffins were at a disadvantage in escaping from gulls (i.e., flat rather than steep slopes) the reproductive success of puffins was significantly lower than in areas away from the gulls.

The literal application of Andrewartha and Birch's general ideas also conflicts with observations on subtle adaptations some waterfowl have made to counter predation.

Barry (1967) described the density-avoiding adaptations of arctic-nesting geese to evade predation—specifically by foxes. Black brant (Branta nigricans) nest on low coastal or delta islands seeking to escape by remoteness. Snow geese (Chen caerulescens) are colonial on large, flat areas, seeking protection in numbers. White-fronted geese (Anser albifrons) are solitary nesters on inland swamps, seeking to be "over-dispersed" among scrub willow.

Common eiders, black scoters (Melanitta nigra), tufted ducks (Aythya fuligula), and other ducks select gull colonies as nesting habitat. Although there is little doubt that the ducks choose gull colonies for nesting, there is some doubt as to the reasons. Finnish biologists (summarized by Bergman 1957; Hildén 1965) have concluded generally that gulls protect the duck nests from predation by hooded crows (Corvus corone).

The Assumption that Fluctuations Are Generally Present

Recently theorists have built models based on assumptions that fluctuations are a general characteristic of population dynamics, such as Gilpin's (1975) model describing multi-phased oscillations. He took account of the fact that fluctuations (and models) become more complex as more species and nonlinear effects are included. May and Leonard (1975) emphasized that the effect of nonlinearities is to make it impossible to speak even in principle of the equilibrium point of a community. They pointed out that even though the model is deterministic (i.e., assumes that the system will come to equilibrium) the oscillations are so complex that they may appear to be random, and it may be a very long time before the system returns to a position near its starting point. "On the other hand a truly random ecological system could always be fitted by a suitably ingenious limit cycle. This suggests that ecological analysis which does not consider component processes must be viewed with great suspicion" (Gilpin 1975). May and Leonard (1975) and Gilpin are both making a familiar point—that neither the logic nor the interactions described in a formula will describe biological reality unless the assumptions are correct. They are also making a different point—that an ingenious mathematician can create a formula to describe almost any operation (whether its workings are systematic or random), and the formula may seem to work.

Gilpin's moral is that one cannot learn very much that is helpful by studying fluctuations as such. One must study the factors controlling populations. This is a very old idea.

It would appear that defining carrying capacity and inherent rate of increase will not be very instructive in managing seabird populations other than in speculating upon what might be ideal upper limits. It can also encourage the musty sophistry that when a population increases beyond this abstract carrying capacity it "needs" to be hunted to prevent overcropping resources and damage to itself through a population decline. But we will not have the time to carry out detailed studies of life histories seeking for critical population-habitat interactions over several fluctuations for each species involved in a disaster before designing programs to help seabird populations to build up their numbers.

General Characteristics of Marine Birds and Waterfowl

Because general theory does not seem to work and because detailed studies take too much time, I conclude that it is necessary to identify certain general principles upon which to base applied programs. These categories of knowledge include: (1) how vulnerable certain categories of seabirds, waterfowl, and shorebirds are to specific types of disasters, (2) how quickly their numbers build up after they have been reduced, and (3) at what stages we can help them best (i.e., at the breeding grounds, at the winter gathering grounds, or on migration). I believe that we already know enough to design effective programs and to begin work. To this end some characteristics of seabirds are identified which determine the population structures and ways in which their numbers respond to changes in the environment.

Habitat

Although the shallow oceans, islands, and seashores are among the most permanent features of the earth in general, the details of their numbers and distribution change rapidly. Sandy shores are obviously being reworked even in the short span of a single lifetime. Distribution of islands and the sediment load, extent, and strengths of currents vary constantly in space and change with time.

The food that seabirds use is patchy and subject to both short-and long-term fluctuations in numbers and shifts in geography. Suitable breeding habitat is scattered, and in many places where oceanic conditions provide a good food supply there are no nesting sites. Consequently, seabirds aggregate in colonies, often dense, and the colonies are clumped for geographical as well as biological reasons.

Lack (1966) discussed some general features of how the breeding adaptations of seabirds are adjusted to the distances the birds must go to find food. The species which feed close to the nest characteristically establish isolated territories or nest in small groups, and they accept many different kinds of nesting substrate. Their clutch sizes are large, individuals move nesting sites readily, and their young grow rapidly compared to the species which feed far at sea. Species which feed far at sea aggregate in large colonies. These species are often rigid in their requirements for suitable nesting sites, their clutches are usually limited to one egg per season, their young grow slowly, and there seems to be strong attachment to traditional colony sites.

Breeding

Ashmole (1963) suggested that the clutch size of some oceanic birds is small and colonies occupy only part of the available habitat because food resources within efficient commuting distance of the breeding site are limited. We can see this effect in the usual failure of common terns to raise a third chick, even in the colonies that are surrounded by favorable habitat (Nisbet 1973). Herring gulls whose colonies are close to sources of human refuse raise more young than do those whose colonies are at some distance (Drury 1963; Kadlec and Drury 1968; Hunt 1972).

Ashmole (1963) suggested that during the course of the breeding season the birds exhaust the available food supply. The validity of this suggestion is reflected in the long distances some species (petrels, boobies, murres, dovekies) go for food to feed their young. One would therefore expect that early nesting pairs would be more successful, and this seems to be the case in herring gulls (Nisbet and Drury 1972), kittiwakes (Coulson 1966), and red-billed gulls, Larus novaehollandiae (Mills 1973).

If food is in short supply and parents have to seek over a wide area for food so that they can bring back only a little food at long time intervals, one would expect these birds to have a small clutch and their young to grow slowly, as is the case. One would also expect seabird colonies situated near oceanic currents to be larger and more successful because food is continuously renewed. Conversely, one would expect colonies next to still waters to be smaller and less successful.

The small clutch size of seabirds means that when a population has been reduced, it will grow slowly toward its former abundance. The growth rates of seabird populations on the New England coast since their release from human predation reflects this. Species such as black guillemots with only two eggs per clutch and herring gulls with three eggs per clutch have increased more slowly than have the populations of common eiders or double-crested cormorants both with three to six eggs per clutch (Drury 1973).

If the species that nest in colonies show a high degree of site tenacity, they are not likely to reestablish a colony after it has been eliminated. An exception to this is the food subsidy provided by man, which seems to have been important in creating a nonbreeding population of herring gulls large enough to form a "critical mass" for the formation of a new gullery.

Age Structure

Because the main element of population size—the number of breeding adults—is limited by the number of breeding colonies and the food available to those colonies, one assumes that the total numbers of seabirds is much less than could be supported by the larger areas of productive oceans. Hence one suspects that there is lessened competition for food outside the breeding season and that lack of competition for food is a major reason for seabirds being long-lived, often to extremes little suspected until recently. Mortalities of 10-12% per year are common, and some as low as 4% (wandering albatross, Diomedea exulans; Tickell 1968) have been recorded.

In contrast, songbirds with large clutches, such as the titmice studied by Kluyver (1951), produce a large number of young with whom they and other adults must compete for food during the winter period of food shortage. Because the titmice are permanent residents, they occupy all of the available habitat throughout the year. Hence titmice suffer intense intraspecific competition, which shortens the survival of adults. Kluyver's experiments (1966) with nest boxes used by a closed population of great tits on Vlieland, The Netherlands, showed that by artificially reducing clutch size the survival of adults was increased.

Similar competition for the few territories available on marshes and consequent shortened life expectancy, can be expected in waterfowl with large broods. The effect should be less marked for geese with smaller clutches that nest in less confined habitats.

The long life span of seabirds means that a population will have a large component of older age categories; this characteristic has several implications:

• It means that the population can survive years of reproductive failure without the observable immediate effects that would be manifest in titmice, grouse, or rabbits. Near failure of reproduction during a breeding season among arctic seabirds at Bear Island was reported by Bertram et al. (1934). Many similar observations have been made since then: Pitelka et al. (1955) reported such a case among skuas and gulls at Point Barrow, Drury (1961) for greater snow geese (Chen cerulescens atlantica) at Bylot Island, Jones (1970) for black brant gathering at Isambek Lagoon on the Alaska Peninsula, and D. A. Snarski (personal communication) for kittiwakes at Cook Inlet. Reproductive failure can sometimes be chronic, as observed by Nisbet (1972) for terns at Cape Cod, Massachusetts, or by Drury (1963) and Hunt (1972) for herring gulls on the outer islands on the coast of Maine.

When reproductive failure becomes chronic as observed on peregrine falcons (Falco peregrinus) by Hickey (1969) and in ospreys (Pandion haliaetus) by Ames and Mersereau (1964), the population of adults may hold on for a number of years without evident decline. Damage to the structure of the whole population may be serious before any numerical results are evident.

• Although there may not be intensive competition for food in the habitat away from breeding colonies, there is intense competition for food and breeding sites at and around the colonies. Hence age and previous experience in seabirds assume importance in establishing territory and in breeding success. Associated with this is the tendency for immature birds to delay breeding until they are several years old and for the immatures to remain on feeding grounds at some distance from the colonies. In some cases young birds may "hang around" breeding colonies and even feed some of the young. When young birds do first breed they usually lay smaller clutches and raise fewer young than do older birds. The importance of age and experience upon breeding success has been well documented for kittiwakes (Coulson 1966) and red-billed gulls (Mills 1973).

The fundamental biological importance of this delayed maturity seems to be emphasized by the persistence for several years of immature plumages, so clearly identifiable that even a human observer can recognize the age of an individual. One assumes such an evident feature must have adaptive significance.

Wintering Grounds

When colonial nesting seabirds leave their breeding islands for their wintering grounds, their identification with that island is lost as far as population effects are concerned, because birds from many colonies mingle on the wintering grounds. Major mortality takes place on the wintering grounds and must therefore act on the species population as a whole rather than differentially on individuals associated with especially dense colonies. Such a direct relation between colony density and mortality would be necessary for density-dependent mortality to regulate the number of birds on a breeding colony. Conversely, one cannot expect that all colonies will decrease equally because mortality should be equally distributed if all the population gathers on a common wintering ground. Thus density-dependence acts only in a very general way upon the sum of animals considered as an abstract entity—the population.

In fact, on the wintering grounds, as shown by a graph of numbers of gulls reported on Christmas Counts on Cape Cod, Massachusetts (Kadlec and Drury 1968), herring gulls are very responsive to local conditions and move several tens of miles to gather at favorable feeding sites. An aerial survey of the gulls on the East Coast of the United States (Kadlec and Drury 1968) showed that more than half of the gulls were gathered near major food sources in large metropolitan districts. Most of the remainder were gathered near small fishing ports. Very few were scattered along the shoreline in what one assumes is the traditional gull habitat. Later analyses of the relation between the distribution of banding recoveries of birds in their first winter and the distribution of immatures as found on this winter census (Drury and Nisbet 1972) suggested that proportionately more first-year gulls died in those areas where the birds were sparsely distributed than died in the crowded metropolitan areas.

These results suggest both that there is not a direct feedback between reproductive rate and mortality, and that mortality may even be inversely density-dependent on wintering grounds. This last runs counter to traditional ecological ideas that density causes a change in mortality rate. The idea that individuals gather where "living is easy" and mortalities are low is consistent with the theory of natural selection. One would not expect the food of the gulls to be evenly distributed, and one would expect individuals to move away from areas where food is scarce and mortality is high.

Differences in Breeding Success Between Colonies

Breeding success has been shown to vary among individual pairs of gulls (Drost et al. 1961). Certain groups of individuals nesting in patches within a single colony have greater breeding success than do others (Coulson 1968; Drury and Nisbet, in preparation). Differences in breeding success also occur between colonies (Frazer-Darling 1938; Kadlec and Drury 1968; Drury and Nisbet 1972). Some colonies reproduce consistently better than others—for example, the gull colonies close to fishing ports and metropolitan areas. Other colonies produce consistently fewer young, such as the colonies on the outer islands in the Gulf of Maine (Drury 1963; Kadlec and Drury 1968; Hunt 1972). The populations of successful colonies grow while the numbers of unsuccessful colonies decline, even during a period of general population increase (Kadlec and Drury 1968).

The difference between success and failure, growth and decline, appears to lie in the food available. Colonies increase where breeding success is high and decrease where breeding success is low. One important reason seems to be that adult gulls may move to a more productive colony even after they have nested with another colony (Drury and Nisbet 1972; Kadlec 1971). Such adaptations can be viewed as adjustments by which individuals meet the requirements of an environment in which the availability of food and other necessities is patchy and shifting.

Dispersal

In general terms, the willingness of some individuals to disperse while the majority of individuals remain loyal to a colony can be considered a major mechanism of population maintenance. If conditions deteriorate seriously at one place so that the local populations decline or disappear, dispersal from other centers can be expected to repopulate the area as soon as local conditions again become suitable. This subject has been treated in more detail by Drury and Nisbet (1972) and Drury (1974b).

Occupation of new, or return to former, nesting sites has been recorded in detail for fulmars (Fulmaris glacialis) by Fisher (1952) and for herring gulls by Kadlec and Drury (1968). Dispersal is also known for waterfowl. Hansen and Nelson (1957) reported that of some 8,000 brant banded in midsummer on the Yukon delta 8 were recovered in northern Siberia and 28 in northern Alaska and arctic Canada. They suspected that pairing on the wintering grounds was responsible for the change in breeding areas, a change that would not be expected among other North American species of geese. Similarly, wide dispersal seems to occur in pintails (Anas acuta), mallards (Anas platyrhynchos), and wood ducks (Aix sponsa).

The general tendency for some individuals to disperse and the frequency of "extra limital" breeding attempts is especially well established in the Bering Sea region, in part at least because vagrants from Siberia or North America are readily identified as such. In the Aleutian Islands, Emison et al. (1971) and Byrd et al. (1974) have enumerated the nesting vagrants. For the Pribilof Islands, Kenyon and Phillips (1965), Sladen (1966), and Thompson and DeLong (1969) have recorded the repeated appearance of birds of Siberian distribution, and Fay and Cade (1959) and Sealy et al. (1971) did the same for St. Lawrence Island.

One can conclude that a few individuals are constantly trying to settle in new geographical areas. As climatic and habitat conditions change, some populations are able to become established; for example, southern species such as mockingbirds (Mimus polyglottus), cardinals (Cardinalis cardinalis), and tufted titmice (Parus bicolor) have settled in southeastern New England during the last 2 decades. These southern species have received much publicity. But at the same time, a less publicized dispersal of white-throated sparrows (Zonotrichia albicollis), hermit thrushes (Catharus guttatus), and dark-eyed juncos (Junco hyemalis) has resulted in new nesting records of more northerly species, also in southeastern New England.

The ability (or lack of ability) of some organisms to expand their ranges over time has been a subject of consideration for a number of years by plant and animal geographers. An important botanical paper on this subject in the Bering Sea region was presented by Hultén (1937), who analyzed the ranges of plants of the area of Kamchatka, eastern Siberia, Alaska, and northwest Canada, showing that diverse floras occur in some restricted geographic areas. He called these areas "refugia," and postulated that many species had survived Pleistocene glaciations in them because these refugia remained ice-free. He, like Fernald (1925), was puzzled as to why only certain species had been able to expand their ranges outward from these "areas of persistence," while other apparently more "conservative" species were unable to do so. Similarly, there appear to be conservative endemic bird species of the Bering Sea region: the extinct Commander Islands cormorant (Phalacrocorax perspicillatus), Steller's eider (Polysticta stelleri), spectacled eider (Lampronetta fisheri), emperor goose (Philacte canagica), whiskered auklet (Aethia pygmaea), least auklet (A. pusilla), parakeet auklet (Cyclorrhynchus psittacula), Aleutian tern (Sterna aleutica), red-legged kittiwake (Rissa brevirostris), bristle-thighed curlew (Numenius tahitiensis), long-billed dowitcher (Limnodromus scolopaceus), surfbird (Aphriza virgata), black turnstone (Arenaria melanocephala), rock sandpiper (Calidris ptilocnemis), and western sandpiper (C. mauri).

The ranges of horned puffins (Fratercula corniculata), Kittlitz's murrelet (Brachyramphus brevirostris) and, perhaps, crested auklet (Aethia cristatella) suggest that some species of "Beringian" seabirds have expanded their ranges from Hultén's (1937) "refugia."

Dispersal and Regional Persistence of Marginal Populations

The presence of several sub-elements of a species population and, therefore, the opportunity for dispersion among alternative breeding sites may be an important factor in the regional persistence of a species on the margin of its range, as illustrated by the history of laughing gulls (Larus atricilla) in New England.

Between 1875 and 1900 there were fewer than 50 laughing gulls in Massachusetts (Mackay 1893) and about 35 in Maine (Norton 1924). In Massachusetts the laughing gulls all settled on one large island, Muskeget, where by 1940 there were about 20,000 pairs (Noble and Würm 1943). Meanwhile, in Maine the population had been disturbed by sheep and men and had shifted about among seven islands. The Maine population grew to only about 350 pairs by 1940 (Palmer 1949).

The laughing gull population in both States has decreased since 1940. In Massachusetts, where all pairs occupied one island, the population had fallen to about 250 pairs by 1972, but the Maine population, still divided into five colonies, stabilized at 250 pairs (i.e., the same as instead of only 1% of the Massachusetts population).

Use of General Principles in Solving Conservation Problems

Game biologists have successfully maintained the populations of hunted animals by using a number of classical principles of game management. They have controlled mortality by regulating kill and have increased standing stock by improving habitat on a local scale. This seems to have worked in species which are short-lived, have large clutch sizes or litters, and which occupy mosaics of highly productive "successional habitat." Seabirds, however, contrast with these species in a number of important biological characteristics. They have small clutches, postpone breeding until they are several years old, and are subject to periodic or chronic reproductive failures. Therefore, their populations are skewed toward older animals and replacement of lost individuals is slow. Many seabirds, like some geese, have a high level of site tenacity and thus may resist recolonization or fail in the attempt to recolonize a breeding site once eliminated from it. In those species studied it appears that the breeding birds at a small percentage of colonies are responsible for a large proportion of the annual crop of young. It is probably dangerous, therefore, to risk either damage to or elimination of well-established colonies.

Studies of kittiwakes by Coulson and White (1958, 1961), sooty terns (Sterna fuscata) by Ashmole (1963) and Harrington (1974), Atlantic puffins by Nettleship (1972), and Cassin's auklets (Ptychoramphus aleutica) by Manuwal (1974), and the practice of eider "farming" in Iceland indicate that the number of available territories or breeding sites may limit the size of a population and that populations can be increased by increasing the number of sites available. This suggests one way in which direct steps can be taken to encourage the numbers of breeding seabirds. Other studies indicate that seabirds will move into synthetic habitat such as created by the window ledges on buildings (Coulson and White 1958) or the islands created by dumping spoil from channel dredging operations (Buckley and Buckley 1971, 1975; Soots and Parnell 1975).

Most generalizations of population biology have been derived from the study of insects, songbirds, or game species. It seems inadvisable to assume that those principles will apply to seabirds without modification. For example, predation by gulls and ravens may have a disastrous effect on a seabird colony at low colony density but have progressively less impact as the colony size and density increase. Fox predation may have important effects over most ranges of prey density because the presence of foxes has important psychological effects.

The habitats of seabirds include elements in which birds are widely dispersed (feeding areas) and others in which birds are crowded and narrowly localized (nesting sites). Thus effective programs of conservation should include guarantees that a number of colony sites be available in as widely dispersed a pattern as possible. Each productive feeding ground should, if possible, have several colony sites available.

We have argued elsewhere (Drury and Nisbet 1972; Drury 1974a) that one of the chief defenses any population has against extinction is the combination of being divided into a number of population centers with having some movement of individuals between the centers, but not too much. Because it is highly improbable that a single catastrophe will affect more than a part of a species' range at any time, the more numerous and widely scattered the partially independent segments of a population are, the better the species is insured against extinction. This, of course, suggests that the size of each colony may be less important for long-term survival than is the total number of colonies.

One intuitively concludes that "conservative" species, such as those endemic to the Bering Sea region (whose dispersal and colonizing mechanisms seem to be poorly developed), are especially vulnerable to the effects of local population crashes. These "local" species therefore deserve special consideration.

I would like to emphasize two points to be included in designing a "management" program:

• It seems that the most promising management techniques will be built upon ensuring the health of colonies and the associated feeding areas at which reproductive success is high enough to "export" young. Thus it is useful to identify those colonies which are exporting young and to give special care to their preservation. As populations of prey species change locally, so will the success of the local nesting birds. A colony which is thriving at one time may be barely maintaining itself at another (Ainley and Lewis 1974), or it may decrease, as in the case of "guano birds" during El Niño years in the Peru Current.

• Because centers of abundance of marine birds shift (Fisher 1952; Drury 1963, 1974a), it will be prudent to plan for large areas and over long periods of time. Harrison Lewis, a pioneer in seabird management in eastern Canada, said (personal communication) that just as soon as he got approval of a new seabird sanctuary through the long corridors of the distant government bureaucracies in Ottawa, the birds would move to a new island and he had to start the process all over again.

The objective is to maintain a variety of colony sites for populations to move among as local patterns of productivity in the shallow sea shift.

Goals for Research on Population Dynamics of Seabirds for Purposes of Conservation

1. To learn the distribution and relative importance of seabird colonies, the number of pairs nesting and nonbreeding individuals at each colony, and the timing of breeding activities for each geographical region. The most important step toward conserving marine birds is to get public ownership and protection for their breeding grounds.

2. To understand the life cycle of key species. Three needs are clear:

a. To identify key species whose biological characteristics can conveniently be studied and measured. Studies of these species may be useful in monitoring the "health" of seabird breeding areas.

If it is established that the reproductive success of certain species varies similarly in response to changes in their marine habitat (such as black-legged kittiwakes and horned puffins), one could use key species (black-legged kittiwake) to assess the performance of those species in a colony whose breeding success is difficult to measure (horned puffin).

b. To develop efficient and practical ways of censusing and measuring productivity of crevice-, scree-, and hole-nesting species such as puffins and auklets.

c. To establish annual differences in reproductive success and mortality rates by age classes of the key species, and from these to identify rates of population turnover so as to be able to predict the effects of mass mortalities.

3. To learn enough about the differences in behavior and productivity among colonies to establish which colonies produce surplus young and which have low productivity. At first, maximum efforts for conservation should be concentrated at those sites which produce surplus young.

4. To learn about colonial behavior. Two needs are apparent:

a. To know enough about the lives of individually marked birds of known age so as to be able to infer the behavior of population elements at all stages of their life cycle.

b. To know enough about the lives of subadult birds to understand what proportion of subadults visit and become established at breeding sites, why the subadults visit the breeding sites and what effect their presence has on the territories and breeding success of their neighbors and biological relatives.

5. To know enough about places where seabirds, waterfowl, and shorebirds gather on migration and during the winter to identify those areas which need special protection from effects of economic development.

a. It is important to determine the areas where marine birds gather at sea when they are away from their breeding grounds. What factors of habitat and food supply make certain places preferable to others? What is the relation between gathering grounds and underwater topography (banks and edges of the continental shelf)? What are the seasonal and annual differences in preferred gathering grounds? What special hazards exist, such as unusual extent of sea ice or exceptional storms?

b. It is important to plot coastal areas where waterfowl and shorebirds gather on migration, for molting, and during the winter. Which open leads in the ice and patches of open water at the mouths of rivers are of especial importance in spring? What shorelines and beaches act as "leading lines" during migration? Which capes and points result in concentrated overflights of migrating waterfowl, and hence are locations of unusually high kills by hunters? What wetlands, bogs, coastal ponds, lakes, and lagoons are used as gathering grounds and to what extent do waterfowl and shorebirds exchange between gathering grounds? How much redundancy of wetlands is needed to make the wetlands system maximally productive for waterfowl and shorebirds?

Answers to these questions will identify which geographic areas deserve special protection during development. The answers will also identify the kinds of influences which might lower the contribution of each critical area to the survival of seabirds, waterfowl, and shorebirds. Areas identified as important under these categories must be included in policy decisions related to land-use planning and management.

6. To learn more about the effects of varying quantities of food on breeding behavior and performance:

a. What are the effects of food abundance in early spring on date of laying, clutch size, and egg size?

b. What effects do storms have at different stages of the reproductive schedule?

c. What effects do quantitative and qualitative (species composition of prey) changes in food supply have on the survival of chicks?

d. What are the similarities and differences between what parents eat and what they feed their chicks?

Although this is important basic biological knowledge, it contributes little to conservation efforts because food differences result from changes in the ocean over which humans can have little effect.

7. To learn more about prey species and their availability to marine birds:

a. To know more about the breeding areas, reproductive rates, growth rates, and routes of dispersal of the major prey food species. In most areas a few species of teleost fish (e.g., Ammodytes) or Crustacea (e.g., copepods, euphausids, mycids, or amphipods) make up most of the food of marine birds. Yet, the barest minimum is known about the biology of such species. A good first estimate of the "condition" of the marine environment can probably be made by measuring reproductive rates and growth rates of these key prey species. Hence an efficient (though indirect) way to measure those rates may be by monitoring reproduction of birds.

b. To know more about the density and distribution of key prey items season by season, and to learn more about the relation of their abundance and distribution to their availability to birds, as Bédard (1969) showed for Calanus to least auklets, and Thysanoessa to crested auklets.

There are some indications that the population size of prey items can vary widely without having a marked effect on the numbers of their predators. Does commercial fishing for the large, predatory fish have a measurable effect on the food available to marine fish? Do the large pollock and salmon fisheries (high seas) make zooplankton available to smaller alcids? Do marine birds affect a fishery?

c. To know more about the oceanography of continental shelf waters, 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.

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[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).

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.

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 1976a, 1976b 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 1976a, 1976b).

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 1975a).

Availability of food varies throughout the year, particularly in marine invertebrates that form the diet of many seabirds (e.g., Spaans 1971; Bédard 1969a). 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 1975a), 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 1975a). 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.

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).

Food type	Kcal/g fresh wt.	Percent fresh wt. composed of:			Digestive efficiency	Kcal metabolizable energy/g fresh wt.
		H2O	Fat	Protein
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 on NE coast	1.1	74	1	16	82	0.9
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 1969b; Nettleship 1972; Sealy 1973a).

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.

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).

Rapidity of wing molt and (indented) flight capability in molt	Timing of start of molt	Species
Slow Retained	During care of young	Cassin's auklet, parakeet auklet (Cyclorhynchus psittacula), whiskered auklet (Aethia pygmaea)
Retained	After young become independent	Least auklet (A. pusilla), crested auklet (A. cristatella)
Rapid Poor	After arrival in winter quarters	Marbled murrelet, Kittlitz's murrelet (Brachyramphus brevirostris)
Almost synchronous None	After end of breeding	Xantus' murrelet (Endomychura hypoleuca)
Synchronous None	As soon as young go to sea	Guillemots (Cepphus spp.), murres, razorbill (Alca torda), dovekie (Alle alle)
None	In winter, after body molt	Puffins

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 1975b). 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 1969a). 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 1973a, 1975b, 1975c). 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.

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).

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 1974a). Overall, the prelaying period is longer for burrow nesters than for those using crevices (Sealy 1973a).

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 1975c), 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).

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 1975a). 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).

Developmental type	Percent yolk (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).

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 (1969a); Cody (1973); Sealy (1973b); Harris (1974); and Manuwal (1974a).

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 1974a).

Nest exposure	Nests destroyed by 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 1974a; Sealy 1975a); 33 h (on the average) in common puffins (Myrberget 1962); 72 h in ancient murrelets, Synthliboramphus antiquus (Sealy 1975a); 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 1969a), 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 1974a). 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.

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 1973b).

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 (1973b). 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 1976a, 1976b). 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).

Fig. 11. Development of thermoregulatory capabilities in nestling double-crested cormorants. From Dunn (1976a). 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 (1975b) 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.

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).

Species	Age when moderate temperature control is attained (days)	Source
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)
Herring gull	2-3	E. H. Dunn (1976b)
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 dougallii)	3	LeCroy and Collins (1972)
Common murre	3	V. V. Rolnik and Yu. M. Kaftonowski (in Sealy 1973b)
Razorbill (Alca torda)	3	V. V. Rolnik and Yu. M. Kaftonowski (in Sealy 1973b)
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 (1974a)
Horned puffin (Fratercula corniculata)	2-6	Sealy (1973a)
Common puffin	6-7	V. V. Rolnik and Yu. M. Kaftonowski (in Sealy 1973b)
Black-legged kittiwake	6-7	V. V. Rolnik, in Belopol'skii (1961)
Double-crested cormorant	14	Dunn (1976a)
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 1973a, 1973b). 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 1973a, 1973b); 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 1973b) 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 1974a).

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).

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).

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.

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 1974b). Others, however, disagree, at least for the breeding season (e.g., Pearson 1968).

Table 6. Life history data for certain northern seabirds.[44]

Species	Annual adult survival (%)	Age at first breeding (years)	Clutch 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 1974b). 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 1974a; 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.

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