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AMER. ZOOL., 20:427-436 (1980) Physiological and Ecological Correlates of Prolonged Incubation in Sea Birds1 G. C. WHITTOW Department of Physiology, John A. Burns School of Medicine, and the P.B.R.C. Kewalo Marine Laboratory, University of Hawaii, Honolulu, Hawaii 96822 SYNOPSIS. Sea birds with long incubation periods are identified, together with the features of their incubation physiology which distinguish them from birds in general. Most sea birds with prolonged incubation are members of the order Procellariiformes. The majority of Pelecaniformes and Charadriiformes with long incubation periods are tropical species. The total amount of water lost from the egg during incubation is a similar fraction of the initial egg weight in sea birds with prolonged incubation as in other birds. The oxygen consumption of the newly hatched chick is similarly related to the chick weight, regardless of the duration of incubation. Within the constraints imposed by these similarities, sea birds with prolonged incubation display a number of adaptations. The daily rate of water loss from the egg, the water vapor conductance of the egg shell, and the total functional pore area of the egg are all relatively low in sea birds with prolonged incubation. The eggs of sea birds with long incubation times are large in relation to the size of the adult bird; in the two species that have been studied, the high energy content of the egg is paralleled by the greater total amount of oxygen consumed during incubation. However, the growth of the embryo is relatively slow in at least one sea bird with a long incubation time, so that prolonged incubation probably entails a comparatively high allocation of energy resources to maintenance requirements. In some species with prolonged incubation, the interval between pipping and hatching is also long and it appears to be a period of great physiological importance. Ecologically, prolonged incubation is associated with either pelagic feeding habits or a tropical environment; both factors may be related to food supply. INTRODUCTION longed incubation is seen as an adaptation to a low rate of acquisition of food. In the present paper, the physiological and ecological correlates of prolonged incubation in sea birds will be examined. "Prolonged incubation" is defined, for this presentation, as an incubation time exceeding the upper 95% confidence limit of the regression line relating incubation time and egg weight, for birds in general (Rahn and Ar, 1974). Table 1 lists the sea birds which have a long incubation time by this criterion. The table is somewhat arbitrary in that some species, which are not included in the Table, have incubation periods close to the 95% confidence limit. In addition, other species which may have long incubation times are not included because their incubation time was not known. Therefore, although there is reasonable assurance that the species included in Table 1 do have long incubation periods, it is possible that there are other sea birds 1 From the Symposium on Physiology of the Avian which also qualify for inclusion. Egg presented at the Annual Meeting of the AmeriTable 1 illustrates the preponderance of can Society of Zoologists, 27-30 December 1979, at Tampa, Florida. Procellariiform species with long incubaDuring incubation, many sea birds travel enormous distances in order to feed and they very often compete for food resources which are relatively scarce. The climatic conditions at their nesting sites may place great demands on their thermoregulatory capabilities and also on their water balance. In many instances, the breeding colonies are completely unprotected by vegetation or by the construction of nests from the extremes of the environment. In addition, the birds may have to compete for limited space. These and other factors have played a part in shaping the incubation patterns of sea birds. Some sea birds have relatively long incubation times. One school of ecological thought (Lack, 1968) accords major importance to the availability of food as a determinant of the duration of incubation. Thus, pro- 428 G. C. WHITTOW relation of Ar and Rahn (1978). It is apparent from Table 2 that the eggshell water-vapor conductance in sea birds with prolonged incubation is lower than the expected value. In the Wedge-tailed Shearwater (Puffinus pacificus), Leach's Petrel (Oceanodroma leucorhoa) and the Red-footed Booby (Sula sula) the ratio of predicted to measured values is 1.7. The water-vapor PHYSIOLOGICAL CORRELATES OF conductance of the shell, like the daily PROLONGED INCUBATION water loss from the egg, is inversely proWater loss from the eggs portional to incubation time, for eggs of Drent (1970), Rahn and Ar (1974), and similar weight. Ar and Rahn (1978) exAr and Rahn (1978) showed that approx- pressed this relationship in the form of a imately 15% of the initial weight of the constant, which has a similar value for freshly laid egg is lost during natural in- most birds, including most sea birds with cubation in a large number of species. This prolonged incubation for which data are weight loss appears to be due largely to available. loss of water from the egg (Drent, 1973; From the measured values for MH 2 O and Rahn and Ar, 1974). Table 2 presents data GH 2 O, the water vapor pressure difference for the fractional weight loss of the eggs of between the egg and its microenvironment sea birds with long incubation times. The (APH 2 O), may be calculated from the relafractional weight loss of the eggs of these tionship of Rahn and Ar (1974). Ar and sea birds varies from 11% in a single egg Rahn (1978) reported an average value of of Sula abbotti and of Phaethon rubricauda 30 torr for the APH 2 O of a large number to 23% in Hydrobates pelagicus. However, of birds. From the limited data contained the mean fractional weight loss of the eggs in Table 2, it may be seen that the APH 2 O is similar to that of other birds. In this for Leach's Petrel (Oceanodroma leucorhoa) sense, the fractional weight loss of the egg and the Red-footed Booby (Sula sula) were constitutes a constraint on incubation. close to this value. However, the APH 2 O for For birds in general, the daily water loss the White Tern (Gygis alba) was lower than from the egg (MH 2 O) may be predicted 30 torr and also less than the mean value from the initial egg weight (Drent, 1970). (27 torr) for a group of seven species of It is clear from Table 2 that, in sea birds terns (Rahn et al., 1976). with long incubation periods, the daily The water-vapor pressure difference water loss is considerably less than the pre- APH 2 O is the difference between the waterdicted values. The highest ratio (2.2) of vapor pressure of the contents of the egg predicted: measured water loss occurred in (PH 2 O egg) and that of the microenvironthe Manx Shearwater {Puffinus puffinus). ment provided by the incubating adult and The daily water loss from the egg is, in the nest (PH 2 O nest). Assuming that the fact, inversely proportional to the length contents of the egg are saturated with of the incubation period for eggs of com- water vapor, the water-vapor pressure of parable size, a relationship that was rec- the egg may be calculated if the egg temognized by Rahn and Ar (1974). The low perature is known. The egg temperature daily water loss from the eggs may be the of some sea birds with long incubation result of either a low value for the con- times (Table 2) is lower than the average ductance of the shell to water vapor (GH 2 O) egg temperature for birds in general or a small difference in water-vapor pres- (36.2°C; Drent, 1975). This is true for the sure between the egg and its microenvi- Wedge-tailed Shearwater and the White ronment (APH 2 O; Rahn and Ar, 1974). Tern, but the petrels have the lowest egg In a large number of birds the water- temperatures. Consequently, the water-vavapor conductance of the shell may be por pressure of the eggs of these species predicted from the egg weight, using the would be relatively low. don times. The members of this order are the most pelagic of all sea birds. The Pelecaniformes are also well represented in Table 1, particularly by the purely tropical forms. In contrast, there are few Charadriiform birds with long incubations: no gulls, only two terns, both tropical species, and one alcid. 429 PROLONGED INCUBATION IN SEA BIRDS TABLE 1. Sea birds with long incubation times.* Order Procellariiformes Species Royal Albatross, Diomedea epomophora Wandering Albatross, Diomedea exulans Black-footed Albatross, Diomedea nigripes Laysan Albatross, Diomedea immutabilis Light-mantled Sooty Albatross, Phoebetria palpebrata Christmas Shearwater, Puffinus nativitatis Short-tailed Shearwater, Puffinus tenuirostris Wedge-tailed Shearwater, Puffinus pacificus Manx Shearwater, Puffinus puffinus Great-winged Petrel, Pterodrorna macroptera Phoenix Petrel, Pterodrorna alba Mottled Petrel, Pterodrorna inexpectata Fulmar, Fulmarus glacialis White-faced Storm Petrel, Pelagodroma marina Dove Prion, Pachyptila desolata Pintado Petrel, Daption capensis Snow Petrel, Pagodroma nivea Wilson's Storm Petrel, Oceanites oceanicus Leach's Storm Petrel, Oceanodroma leucorhoa Madeiran Storm Petrel, Oceanodroma castro Fork-tailed Storm Petrel, Oceanodroma furcata British Storm Petrel, Hydrobates pelagicus Pelecaniformes Abbott's Booby, Sula abbotti Red-footed Booby, Sula sula Brown Booby, Sula leucogaster Masked Booby, Sula dactylatra Peruvian Booby, Sula variegata Great Frigate-bird, Fregata minor Andrew's Frigate-bird, Fregata andrewsi Lesser Frigate-bird, Fregata ariel Red-tailed Tropic Bird, Phaethon rubricauda Red-billed Tropic Bird, Phaethon aethereus White-tailed Tropic Bird, Phaethon lepturus Charadriiformes Cassin's Auklet, Ptychoramphus aleuticus White Tern, Gygis alba White-capped Noddy, Anous tenuirostris Measured incubation time (days) Predicted incubation time (days) 79 78 65 64 65 54 53 52 51 53 53 50 49 46 45 44 43 43 42 38 45 46 41 41 39 30 32 29 29 31 29 29 33 21 26 30 37-68 41 57 45 45 43 42 55 54 45 44 43 41 38 36 35 28 19 20 20 21 18 33 29 30 30 29 32 31 29 30 30 27 25 23 24 * Only species in which the measured incubation time exceeds the 95% confidence limit of the predicted value (based on the egg weight; Rahn and Ar, 1974) are shown. The table is based on information presented by Lack (1968), Nelson (1968, 1969, 1971, 1976), Warham et al. (1977), Ar and Rahn (1978), Rahn (personal communication) and Boersma and Wheelwright (1979). If the egg water-vapor pressure (PH 2 O dicted by Ar et al. (1974). The eggs of the egg) and the water vapor pressure differ- two Procellariiform species {Puffinus pacience (APH 2 O) are known, the water-vapor ficus, Oceanodroma furcata) tended to have pressure in the nest microenvironment a thin shell, and, therefore, a relatively (PH 2 O nest) may be calculated. Such cal- short pore length, while the eggs of the culations, for sea birds with long incuba- two sulids (Sula sula, Sula leucogaster) had tion periods (Table 2), reveal some consid- thicker shells than those predicted on the erable diversity of values. basis of egg mass (Ar et al., 1974). In Table 3, the calculated values for the Functional properties of the shell total functional pore area of the eggs of In Table 3, the measured shell thickness the sea birds under consideration, are of sea birds with long incubation periods compared with the areas predicted for is presented together with the value pre- birds in general. The functional pore area 430 G. C. WHITTOW TABLE 2. Factors affecting water-loss from the eggs of sea birds with long incubation times. a IH,O (mg •day Species Diomedea exulans Diomedea nigripes Diomedea immutabilis Puffinus pacificus Puffinus puffinus Pterodroma inexpectata Pterodroma hypoleuca hypoleuca Oceanodroma leucorhoa Oceanodroma furcata Hydrobates pelagicus Bulweria bulwerii Sula abbotli Sula sula Sula leucogaster Fregata minor Phaethon rubricauda Ptychoramphus aleuticus Gygis alba Anous tenuirostris a GH 2 O 1 F (%) Measured ) Pre- 6 dicted 16 1050 1495 15 14 12 18 750 155 140 220 90 46 54 40 77 965 299 303 315 190 18 15 23 11 16 11 12 16 199 101 74 106 (mg-day" '•torr"1) PreMeasured dict edc (°C) e gg' (torr) PHO nest (torr) APH,O (torr) 36.4 36.0 35.0 46 42 18 24 45.5 6.4 10.6 87 103 63 1.5 2.1 2.6 3.2 32.5 37 6 31 26 287 5.8 7.6 9.9 36.0 45 12 33 11.9 11.9 36.8 36.0 47 45 24 6.1 4.6 5.1 35.4 37.4 43 48 22 25 21 25 21 23 333 186 145 156 9.6 4.1 3.5 4.5 F = (weight loss during incubation/initial egg weight) x 100; MH2O = daily water loss from the egg; GH2O = water-vapor conductance of the shell; TeBg = egg temperature; Pn.2o, egg = water-vapor pressure of egg contents; PH 2 O, nest = water-vapor pressure of the microenvironment of the egg; APH.2O = PH2O, egg - PH2O, nest. "Drent (1970). c Ar and Rahn (1978). This table is based on Howell and Bartholomew (1961), Fisher (1969), Nelson (1971), Tickell (1968), Rahn et al. (1976), Warham et al. (1977), Ar and Rahn (1978), Ricklefs and Rahn (1979), Ackerman el al. (1980), Rahn (personal communication), Vleck and Kenagy (1980), Whittow et al. (unpublished). was lower than the expected area in all longed incubation are also subject to the species with long incubation times; in the same limiting gas tensions in their air cells. Fork-tailed Petrel {Oceanodromafurcata) the Unfortunately, the composition of the gas pore area was only 52% of the expected in the air cell has not been measured diarea. In the three species for which data rectly in other sea birds with long incubaare available, the low total functional pore tion times. Vleck et al. (1979) have sugarea was associated with fewer pores in the gested recently that the partial pressure of egg shell (Table 3). oxygen in the air cell of small altricial species may be considerably lower than Air cell gas tensions 1 0 0 t o r r shearwaters are considered to be As the embryo grows, it uses oxygen and intermediate between the precocial and produces carbon dioxide. These changes altricial condition (Dawson and Hudson, are reflected in the composition of the gas 1970); it would be illuminating to know the in the air cell; the partial pressure of oxy- gas tensions in the air cell of altricial sea gen (Po2) falls and that of carbon dioxide birds with long incubation times. (Pco2) rises. In the eggs that have been examined, the Po2 diminishes to a mean val- Oxygen conductance of the shell and ue of 104 torr, while the Pco2 rises to 37 shel1 membranes torr before pipping of the shell over the The composition of the gas in the air cell air cell occurs (Rahn et al., 1974). Similar is determined by the gas conductance of levels of gas tensions occur in the Wedge- the shell and shell membranes on the one tailed Shearwater egg (Ackerman et al., hand, and the oxygen consumption of the 1980), suggesting that birds with pro- embryo, on the other. The low water-va- 431 PROLONGED INCUBATION IN SEA BIRDS TABLE 3. Properties of the eggshell of sea birds with long incubation times." Ap(mma) L(mm) Species N Measured Predicted" Calculated" Predicted" Measured Predicted1 0.27 0.33 0.77 1.36 3747 1430 8032 3905 0.14 0.36 0.39 0.36 0.17 0.19 0.17 0.32 0.35 0.35 0.17 0.22 0.12 0.89 1.33 1.54 0.26 0.38 0.23 1.26 1.69 1.68 0.41 0.46 3295 6020 Puffinus pacificus Oceanodroma leucorhoa Oceanodroma furcata Sula sula Sula leucogasler Phaethon rubricauda Gygis alba Anous tenuirostris Ptychoramphus aleuticus a L = shell thickness; Ap = total functional pore area; N = no. of pores per egg. Ar etal. (1974). Tullett and Board (1977). This table is based on Rahn et al. (1976), Ar and Rahn (1978), Rahn (personal communication), Vleck and Kenagy (1980), Whittow et al. (unpublished). b c por conductance of the shell in birds with long incubation periods (Table 2) implies that the oxygen conductance (Go2) of the shell and shell membranes is also low, as the conductances are proportional to the respective diffusion coefficients of water vapor and oxygen (Paganelli et al., 1978). In the Wedge-tailed Shearwater, the low value for Go 2 , calculated from the measured GH 2 O and known diffusion coefficient for oxygen, was close to the value for Go2 determined experimentally from measurements of the oxygen uptake of the egg and the oxygen pressure difference between the air in the air cell and that surrounding the egg (Ackerman et al., 1980). Oxygen uptake of the embryo According to Vleck et al. (1979), the oxygen consumption in altricial species increases throughout incubation. In precocial species, the oxygen consumption increases to a plateau, while in ratite birds the oxygen consumption increases to a peak value and then declines prior to pipping (Hoyt et al., 1978). In the Wedgetailed Shearwater the oxygen consumption increases to a plateau immediately prior to pipping (Ackerman etal., 1980), but in the Fork-tailed Petrel, another procellariiform bird with a long incubation period, there was no evidence of a plateau (Vleck and Kenagy, 1980). Rahn et al. (1974) established a relationship between the oxygen uptake (Mo2) im- mediately prior to pipping and fresh egg weight in a number of species of birds. This relationship was extended by Hoyt et al. (1978) to include two species of ratites. The oxygen consumption immediately prior to pipping in the Wedge-tailed Shearwater was considerably below the value predicted by this relationship. The oxygen consumption of Leach's Petrel, at a comparable time during incubation, may also be low (Rahn, personal communication). However, the measured and predicted values for the Fork-tailed Petrel were very close (Vleck and Kenagy, 1980). The reasons for this difference between the Fork-tailed Petrel on the one hand, and the Wedge-tailed Shearwater on the other, require elucidation. Pipping-hatching interval The first appearance of small starshaped fractures of the shell (pipping) of the Wedge-tailed Shearwater occurs on the 47th day of incubation. This means that the interval between pipping and hatching is approximately five days—considerably longer than in the domestic fowl (Whittow and Pettit, unpublished observations). Penetration of the air cell by the embryo's beak occurs 1-2 days after pipping and, approximately 2 days before hatching, a definite hole is made in the shell. The implications of the Shearwater's long pipping-hatching interval for water loss and oxygen consumption are considerable. 432 G. C. WHITTOW TABLE 4. Pipping-hatching interval in six species ofprocellariiform birds with long incubation times. Pippinghatching interval (days) Species Wedge tailed Shearwater (Pufjinus pacificus) 5.2 Grey-faced Petrel (Pterodroma macroptera Gouldi) 5 Mottled Petrel (Pterodroma inexpectata) 4.2 Bulwer's Petrel (Bulweria bulwerii) 4 Laysan Albatross (Diomedea immutabilis) 3.2 Black-footed Albatross (Diomedea nigripes) 3 This Table is based on Rice and Kenyon, (1962); Imber, (1976); Warham et al. (1977); Ackerman el al. (1980); and Whittow and Pettit (unpublished observations). Thus, the daily rate of water loss from the pipped egg is greater than that from the unpipped egg, and the water loss from an egg in which a hole has been made is even greater. These measured values are not unexpected, because once the shell is cracked, the integrity of the barrier to diffusion of water vapor and oxygen is lost. Although the pipping-hatching interval is long in absolute terms, it accounts for less than 10% of the Shearwater's entire incubation period. Yet 28% of the total water loss from the egg occurs between pipping and hatching. The figures for oxygen consumption are even more impressive: No less than 44% of the total oxygen consumed by the egg is taken up between pipping and hatching. After the embryo has TABLE 5. Oxygen uptake (Vo2) of the newly hatched chicks of sea birds with long incubation times. Species No. of chicks Puffinus pacificus Oceanodroma leucorhoa Oceanodroma furcata 12 1 2 Body weight Vo, (ml .day ') (gi Measured Predicted* 39.10 6.31 7.54 840 308 264 900 238 271 * Ackerman et al. (1980). This table is based on the data of Ackerman et al. (1980) and Vleck and Kenagy (1980). made a hole in the shell, and possibly before this stage, it ventilates its lungs. Pulmonary ventilation may be necessary to elevate the level of oxygen consumption prevailing in the embryo at the time of pipping to that of the hatchling (see below). The incidence of a long pipping-hatching interval in sea birds with prolonged incubation is not known. It may be common in Procellariiform birds (Table 4). Oxygen uptake of the hatchling In ten species of birds, the oxygen consumption (Vo2) of the newly hatched chick could be represented by the relationship of Ackerman et al. (1980). Information on the oxygen consumption of hatchlings of sea birds with prolonged incubation are scant, and they are available only for Procellariiform birds (Table 5). There is no clear evidence from these data that prolonged incubation has resulted in any adaptation in the overall metabolic rate of the hatchling. This implies that the developing embryo has to achieve a given level of oxygen consumption related to its weight by the time that it hatches, regardless of the duration of incubation. In this sense, the level of oxygen consumption of the chick at hatching is a constraint on the events which precede hatching. Growth of the embryo It might be expected that both the relatively early onset of pipping and the low level of oxygen consumption immediately prior to pipping in the Wedge-tailed Shearwater embryo would have implications for the growth of the embryo. This expectation was realized; the embryonic wet weight of the Shearwater immediately prior to pipping was only 24 g, as opposed to 28-29 g for the domestic fowl (Ackerman et al., 1980). The maximal daily weight gain in the Shearwater was 1.4 g/ day while that of the domestic fowl was 3.5 g/day. The energetics of prolonged incubation Although the pre-pipping stage of incubation takes considerably longer in absolute terms in the Wedge-tailed Shearwater than in the domestic fowl, the total PROLONGED INCUBATION IN SEA BIRDS amount of oxygen consumed in the two species, is the same (4.3-4.6 liters O2; Ackerman etal., 1980). Apparently the longer pre-pipping period in the Shearwater is compensated for by the lower rate of oxygen consumption of the Shearwater embryo. However, as the Shearwater embryo is smaller than that of the domestic fowl at the time of pipping (see above), it follows that the oxygen cost of producing a gram of embryonic tissue is higher in the Shearwater. The post-pipping, pre-hatching period in the Shearwater is not only longer but the increase in the rate of oxygen consumption during this period is considerably greater than in the domestic fowl. The net effect of these changes is that the total amount of oxygen consumed over the entire incubation period is greater in the Shearwater (ca. 8 liters O2). When these amounts of oxygen are related to the wet weight of the hatchling, it transpires that the oxygen cost of producing a unit weight of hatchling tissue is also greater in the Shearwater. Vleck and Kenagy (1980) found that in the Fork-tailed Petrel also, the total amount of oxygen consumed over the entire incubation period was much greater than that predicted for birds in general (Ar and Rahn, 1978). Presumably, the longer the incubation period, the greater the total amount of oxygen required, possibly to meet the maintenance requirements of the embryo. The higher amount of oxygen consumed by the Shearwater and Petrel embryos over their entire incubation periods implies that there is a greater store of metabolic substrate in the freshly-laid egg. The yolk-albumen ratio (0.69) in the Shearwater egg is in fact higher than that in the domestic fowl's egg. It might be expected, from these considerations, that the higher total amount of energy expended during prolonged incubation, and the greater amount of substrate, would be reflected also in the greater size of the egg. Vleck et al. (unpublished) have drawn attention to the linear relation between initial egg weight and the total energy expenditure during incubation. In addition, Lack (1968) and Rahn et al. (1975) have shown that Procellariiform 433 birds lay larger eggs for a given body weight than do any other avian order. A relationship between the relative size of the egg and duration of incubation is evident also within orders. Thus in the Sulidae, the egg of Abbott's Booby, which has by far the longest incubation period, is a greater percentage of the weight of the adult female bird, than in other species which have shorter incubation periods (Nelson, 1971). Abbott's Booby is, in fact, the only sulid in which the egg weight is a higher percentage of the adult's weight than would be expected from the adult weight (Rahn et al., 1975). A larger egg is also a prerequisite of the precocial condition of the hatchling (Dawson and Hudson, 1970); other things being equal, the more developed the embryo is at hatching, the greater the amount of material that must be incorporated in the egg. Consequently, birds with long incubation periods and well developed hatchlings would be expected a priori to have the largest eggs, a situation approached by Procellariiform birds. Presumably in the boobies, the long incubation period of Abbott's Booby is a more influential factor affecting the relative size of the egg than is the altricial condition of the hatchling. ECOLOGICAL CORRELATES OF PROLONGED INCUBATION If the duration of incubation is related to the rate at which food can be delivered to the nesting site, as might be inferred from Lack's (1968) arguments, then pelagic sea birds would be expected to have long incubation periods simply because the birds travel greater distances in order to obtain their food. This generalization is certainly applicable to Procellariiform birds, which all have long incubations and are pelagic. There are exceptions, however, among the Pelecaniformes. Whereas all three species of tropic birds are both pelagic and have prolonged incubation, one sulid, the Brown Booby (Sula leucogaster), is an inshore feeder but it has a long incubation time. Of the three species of Charadriiform birds included in Table 1, the White-capped Noddy (Anous tenuirostris) has a long incubation time but it is an 434 G. C. WHITTOW inshore feeder. The White Tern (Gygis alba), which also has a long incubation time, has been reported to be a pelagic feeder in some areas but not in others (Diamond, 1978). Cassin's Auklet is an offshore feeder. The Sooty Tern (Sterna fuscata), on the other hand, is one of the most pelagic of all sea birds, but its incubation is not prolonged. The relationship between pelagic feeding and long incubation time is clearly not a simple one. As Diamond (1978) has pointed out, pelagic birds may be compensated for the greater distances that they have to travel in order to procure food by the reduced competition for food resources and by utilization of areas of high food density distant from shore. Many of the species listed in Table 1— all of the Pelecaniformes and two out of three Charadriiform species—are tropical sea birds. This again may be related to the food supply of the birds: Tropical oceans are noted for the scarcity of their food resources (Lack, 1967), and prolonged incubation in tropical sea birds may be an adaptation to the rate at which food can be acquired. Among the Procellariiformes, the incubation periods of the tropical species are not greater, in relation to predicted values based on egg weight, than are those of members of the Order which occur in higher latitudes. Nevertheless, the eggs of tropical Procellariiformes tend to be proportionately larger (Lack, 1968), and this again may be related to food supply. However, in this particular instance, the larger egg may make provision, not for a longer incubation period, but for a greater supply of food, in the form of yolk, to the hatchling. The tropical environment also places thermoregulatory demands on the incubating birds. A tropical sea bird may be required to respond to heat stress in an appropriate behavioral manner, and this behavior may affect the egg temperature or water-vapor pressure in the microenvironment of the egg. Both within and between orders, sea birds with long incubation times display striking differences in their nesting habits. Among the Procellariiformes, for example, the smaller members—the petrels and shearwaters—nest in burrows, which can be both long and deep. While the burrows may absolve the adult birds from meeting thermoregulatory requirements, they would be expected to permit the accumulation of moisture and carbon dioxide in the microenvironment of the egg. Other things being equal, this might favor a long incubation, because of the reduced differences in oxygen, carbon dioxide, and water vapor pressure across the eggshell. In consonance with this, the incubation times of the small, burrow-nesting Procellariiformes are relatively longer than those of the larger, surface-nesting members. Among the Pelecaniformes, the two species with the longest incubation times are Abbott's Booby which constructs a nest in trees, and the Great Frigate Bird which builds a nest in bushes. Similarly, the incubation period of the bush-nesting Redfooted Booby is relatively greater than that of the Brown Booby and the Masked Booby, which lay their eggs on the bare sand. However, in the Charadriiformes, the White-capped Noddy and the White Tern have almost identical incubation time, although the former constructs an elaborate nest in trees while the latter lays its egg precariously on the branch of a tree, with no pretense at a nest. The White-capped Noddy has the larger egg and, a priori, would be expected to have the longer incubation period. The absence of predators is conducive to the evolution of a long incubation period (Drent, 1975). The presence of predators at the nesting site is a compelling reason for accelerating the incubation time in order to reduce the period of vulnerability of the birds and their eggs. Shallenberger (1973) has discussed the incidence of predation in the Procellariiformes; some species are subject to predation while others encounter predation in some areas but not in others. Burrow-nesting shearwaters and petrels are safe from avian predators, but not from rats. It is difficult to discern whether predation has influenced the incubation period, partly because predation, in many instances, is a relatively recent event. Many of the Pelecaniformes with prolonged incubation nest in bushes or PROLONGED INCUBATION IN SEA BIRDS trees and they are therefore relatively secure from predation. This is also true of the two tropical terns. There may, therefore, be a connection between prolonged incubation in these tropical species and freedom from predation. Another analogous factor is the pressure exerted by other species of sea birds at the nesting site. Thus, Shallenberger (1973) has commented on the effect of Sooty Terns on the Wedge-tailed Shearwaters of Manana, in the Hawaiian Islands. The two species share the same area and their breeding cycles overlap. While the connection between these events and incubation periods has not been established, they have the potential of influencing incubation, by an effect on either its duration or the time of year at which the eggs are laid. One technique for securing prolonged incubation, which has physiological and behavioral as well as ecological connotations, was touched on by Vleck and Kenagy (1980). The egg of the Fork-tailed Petrel is often temporarily deserted by both parents. This results in cooling of the egg, arrested development and, consequently, prolongation of incubation. As Vleck and Kenagy pointed out, however, desertion of the egg is effective in prolonging incubation only if the burrow temperature is sufficiently low (10°C in the case of the petrel) to reduce the oxygen consumption of the embryo to a small fraction of that of the incubated egg. Otherwise, the embryo would continue to develop and there would be only a relatively small extension of incubation time. This implies that periodic desertion of the egg would be less effective in prolonging incubation in tropical sea birds than in colder climates. The rate of cooling of the egg is related also to its size; a small egg would cool more rapidly than a large one (Kendeigh, 1973). It may not be coincidental therefore that cooling of the egg, associated with prolonged incubation in sea birds, has been described only in those Procellariiformes which have small eggs. Long incubation times in sea birds are associated with other features which, although they lie outside the scope of the present review, nevertheless, merit passing 435 mention. Long incubation times are often related to small clutches and long incubation spells by each parent before being relieved by the other (Lack, 1968). The fledging period, like the incubation period, may be prolonged. Some of these correlates of prolonged incubation may also be related to food supply; others await further elucidation. ACKNOWLEDGMENTS The preparation of this paper, and some of the scientific work related to it, were supported by a grant (PCM 76-12351) from the National Science Foundation. The acquisition of original data reported herein would not have been possible without the permission and assistance of Mr. Thomas Cajski, Environmental Specialist, Kaneohe Marine Corps Air Station, the State of Hawaii Division of Fish and Game, the U.S. Fish and Wildlife Service, and the National Marine Fisheries Service. I am grateful to Dr. Hermann Rahn and Dr. Carol M. Vleck, and their coauthors, for permission to use their data before they were published. REFERENCES Ackerman, R. A., G. C. Whittow, C. V. Paganelli, and T. N. Pettit. 1980. Oxygen consumption, gas exchange and growth of embryonic Wedgetailed Shearwaters (Puffinus pacificus chlororhyn- chus). Physiol. Zool. (In press) Ar, A., C. V. Paganelli, R. B. Reeves, D. G. Greene, and H. Rahn. 1974. The avian egg: Water vapor conductance, shell thickness, and functional pore area. Condor 76:153-158. Ar, A. and H. Rahn. 1978. Interdependence of gas conductance, incubation length and weight of the avian egg. In J. Piiper (ed.), Respiratory function in birds, adult and embryonic. Springer-Verlag, Berlin. Boersma, P. D. and N. T. Wheelwright. 1979. Egg neglect in the Procellariiformes: Reproductive adaptations in the Fork-tailed Storm-petrel. Condor 81:157-165. Dawson, W. R. and J. W. Hudson. 1970. Birds. In G. Causey Whittow (ed.), Comparative physiology of thermoregulation, Vol. 1. Academic Press, New York. Diamond, A. W. 1978. Feeding strategies and population size in tropical sea-birds. Amer. Natur. 112:215-223. Drent, R. H. 1970. Functional aspects of incubation in the Herring Gull. Behaviour, Suppl. 17:1 — 132. Drent, R. H. 1973. The natural history of incuba- 436 G. C. W H I T T O W tion. In D. S. Farner (ed.), Breeding biology of birds. tion in birds, adult and embryonic. Springer-Verlag, Nat. Acad. Sci., Washington, D.C. Berlin. Drent, R. H. 1975. Incubation. In D. S. Farner and Rahn, H. and A. Ar. 1974. The avian egg: Incubation J. R. King (eds.), Avian biology, Vol. 5. Academic time and water loss. Condor 76:147-152. Press, New York. Rahn, H., C. V. Paganelli, and A. Ar. 1974. The avian egg: Air-cell gas tension, metabolism and Fisher, H. I. 1969. Eggs and egg laying in the Laysan incubation time. Respir. Physiol. 22:297-309. Albatross, Diomedea immutabilis. Condor 71:102— Rahn, H.,C. V. Paganelli, and A. Ar. 1975. Relation 112. of avian egg weight to body weight. Auk 92:750Howell, T. R. and G. A. Bartholomew. 1961. Tem765. perature regulation in Laysan and Black-footed Albatrosses. Condor 63:185-197. Rahn, H., C. V. Paganelli, I. C. T. Nisbet, and G. C. Whittow. 1976. Regulation of incubation water Hoyt, D. F., D. Vleck, and C. M. Vleck. 1978. Meloss in eggs of seven species of terns. Physiol. tabolism of avian embryos: Ontogeny and temZool. 49:245-259. perature effects in the ostrich. Condor 80:265— 271. Rice, D. W. and K. W. Kenyon. 1962. Breeding cycles and behavior of Laysan and Black-footed Imber, M. J. 1976. Breeding biology of the GreyAlbatrosses. Auk 79:517-567. faced Petrel Pterodroma macroptera gouldi. Ibis 118:51-64. Ricklefs, R. E. and H. Rahn. 1979. The incubation temperature of Leach's Storm Petrel. Auk Kendeigh, S. C. 1973. The natural history of incu96:625-627. bation. Discussion. In D. S. Farner (ed.), Breeding biology of birds. Nat. Acad. Sci., Washington, D.C. Shallenberger, R.J. 1973. Breeding biology, homing behavior, and communication patterns of the Lack, D. 1967. The natural regulation of animal numWedge-tailed Shearwater, Puffinus pacificus chlobers. Oxford. Lack, D. 1968. Ecological adaptations for breeding in rorhynchus. Ph.D. Diss., University of California, Los Angeles. birds. Methuen, London. Nelson, J. B. 1968. Galapagos, islands of birds. Long-Tickell, W. L. N. 1968. The biology of the great albatrosses, Diomedea exulans, and Diomedea epomans, London. mophora. Antarctic Res. Ser. 12:1—55. Nelson, J. B. 1969. The breeding biology of the Redfooted Booby in the Galapagos. J. Anim. Ecol. Tullett, S. G. and R. G. Board. 1977. Determinants of avian eggshell porosity. J. Zool. (London) 38:181-198. 183:203-211. Nelson, J. B. 1971. The biology of Abbott's Booby, Sulaabbotti. Ibis 113:399-467. Vleck, C. M., D. F. Hoyt, and D. Vleck. 1979. Metabolism of avian embryos: Patterns in altricial Nelson, J. B. 1976. The breeding biology of frigateand precocial birds. Physiol. Zool. 52:363-377. birds—a comparative review. Liv. Bird 14th: 113Vleck, C. M. and G. J. Kenagy. 1980. Embryonic 156. metabolism of the Fork-tailed Storm-petrel: PhysPaganelli, C. V., R. A. Ackerman, and H. Rahn. iological patterns during prolonged and inter1978. The avian egg: In vivo conductances to rupted incubation. Physiol. Zool. 53:32—42. oxygen, carbon dioxide and water vapor in late development. In J. Piiper (ed.), Respiratory func- Warham, J., B. R. Keeley, and G. J. Wilson. 1977. Breeding of the Mottled Petrel. Auk 94:1-17.