Download Physiological and Ecological Correlates of

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.
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