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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

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).

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.

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.

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).

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.

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).

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.

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).

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).

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).

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).

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).

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.