AMER. ZOOL., 20:437-447 (1980)
Adaptations to Underground Nesting in
Birds and Reptiles1
ROGER S. SEYMOUR
Department of Zoology, University of Adelaide,
Adelaide, South Australia 5000
AND
RALPH A. ACKERMAN
Physiological Research Laboratory, Scripps Institution of Oceanography,
La folia, California 92093
SYNOPSIS. Most bird eggs have evolved a suite of remarkably consistent adaptations for
appropriate exchanges of respiratory gases and water vapor during incubation in nests
above ground. However, underground incubation is associated with selective forces different from those operating at the surface. New information from mound-building birds,
living reptiles and extinct dinosaurs shows convergent adaptations to nest atmospheres
that are high in CO2, low in O> and nearly saturated with water vapor. High humidity
eliminates the danger of excessive dehydration, so gas conductance of the eggshell may
be higher than normal, as a compensation for the unusual nest gases. In contrast with
embryos of birds that next above ground and initiate breathing inside the shell, those of
megapode birds lack an aircell and can breathe only after the shell is broken. Extreme
precocity of megapode chicks is related to long incubation time and large energy stores
in the egg. Because the material around a buried nest restricts diffusion, the size of the
nest must be limited to prevent intolerable gas tensions adjacent to the eggs. This effect
may have forced certain large reptiles to separate their layings into several clutches and
some megapodes to actively ventilate their mounds.
INTRODUCTION
Natural selection of birds nesting on or
above ground has resulted in a remarkably
consistent suite of adaptations that provide
appropriate exchanges of respiratory gases and water vapor across the shell (Ar and
Rahn, 1978). Because there is a large body
of information on gas exchange in eggs
laid in an aerial environment, we can now
appreciate the adaptive compensations to
unusual nesting conditions.
Birds of the family, Megapodiidae, incubate their eggs in mounds or simple excavations beneath the ground. They share
this behavior with certain reptiles, chiefly
crocodilians and chelonians, that also construct incubation mounds or subterranean
chambers. Isolated from the free atmosphere, the embryos must develop under
conditions that depart from those experienced by most bird eggs above ground.
The gaseous environment of buried eggs
is characterized by high humidity as well
as high CO2 and low O2 tensions. The nest
atmosphere depends not only on the rates
of respiration of the eggs, but also on the
decomposition of organic matter and the
resistance to diffusion in the material surrounding the eggs.
In this report, we examine the behavior
and physiology of underground nesting in
birds and reptiles, considering the conditions experienced by the developing embryos and some of the adaptations to subterranean life.
MEGAPODE BIRDS
The nests
There are 13 species of I ndo-Pacific megapodes, but only two Australian species
have produced significant information on
incubation biology. This is regrettable because of the extreme variability of nest environments, ranging from excavations in
sand heated by the sun or geothermal ac1
From the Symposium on Physiology of the Avian
Egg presented at the Annual Meeting of the Ameri- tivity to mounds of forest litter heated by
can Society of Zoologists, 27-30 December 1979, at organic decomposition (Frith, 1962). ForTampa, Florida.
tunately, there is information about the
438
R. S. SEYMOUR AND R. A. ACKERMAN
TABLE 1. Respiratory parameters of buried megapode eggs compared to predictions from other bird eggs incubated above
ground.
Brush Turkey
{AUctura tathami)
Parameter
Predicted
Mean
Incubation temperature, °C
Nest Po2, torr
Nest Pco2, torr
Egg weight, g
Shell thickness, mm
Water vapor conductance, mg/day torr
Functional pore area, mm2
Incubation time, days
Pre-hatching O2 consumption, ml/day
Mallee Fowl
I[Leipoa ocelUUa)
37.3
35.7
136"
100
62
203
a
8"
60 c
0.58d
21.3e
7.41*
0.34
47.3
6.87'
h
49
38'
1433
1106
k
Mean
Predicted
34
126
29
170
0..27
21 .4
35.7"
136"
2..47'
6211
1350
8"
60 c
0.53d
15.9°
5.94"
37'
732k
Data from Seymour and Rahn (1978) and Seymour, Vleck and Vleck (unpublished) unless otherwise noted:
Drent(1975).
Calculated from nest ventilation and gas exchange data of Rahn el al. (1974, 1976).
c
1800 g Galliform bird, Lack (1968).
d
Equation 7, Ar el al. (1974).
e
Equation 4, Ar and Rahn (1978).
' Equation 5, Ar el al. (1974).
8
Equation 9, Ar and Rahn (1978).
h
Baltin (1969).
'Frith (1959).
1
Equation 1, Rahn and Ar (1974).
k
Equation 4, Rahn et al. (1974).
a
b
mounds and eggs of the Brush Turkey gle egg of the Maleo Bird (Megacephalon
(Alectura lathami) which uses organic de- maleo) to the mounds of Scrub Fowl (Mecomposition only (Fleay, 1937; Baltin, gapodius freycinet) which may exceed 10 m
1969; Seymour and Rahn, 1978), and the in diameter and 4 m in height (Frith,
Mallee Fowl (Leipoa ocellata) which supple- 1962). The size of the mound is related to
ments solar radiation with organic heat the degree of reliance on organic decom(Frith, 1955, 19566, 1957, 1959, 1962; Sey- position as a heat source. Mounds are not
normally formed by species employing somour, Vleck, and Vleck, unpublished).
Megapode nests vary in size and shape lar radiation or vulcanism as the sole
from simple pits in sand containing a sin- source of heat.
TABLE 2. Collected nesting data for large underground or mound nesting reptiles.
Approx.
mass
(kg)
Clutch
size
# eggs
400
150
136
34
30
88
113
120
160
111
7.1
5.5
4.5
5.2
3.7
Alligator mississippiensu
62
40
2.6
Crocodylus porosus
Crocodylus niloticus
Crocodylus novaeguineae
Crocodylus aculus
Crocodylw, palustris
200
200
50
127
100
50
60
29
56
41
5.6
Species
Clutch
mass
kg
Nest
temp,
°c
Incubation
time
(days)
Reference
Sea Turtles
Dermochelys coriacea
Chelonia mydas
Caretta caretta
Eretmochelys imbricata
Lepidochelys olivacea
65
58
55
62
51
Ackerman,
Ackerman,
Ackerman,
Ackerman,
Ackerman,
28-30°
64
27-31°
28-30°
36-38°
85
Seymour, 1979; Neil, 1971;
Joanen, 1969
Seymour, 1979; Xeil, 1971
Seymour, 1979; Xeil, 1971
Neil, 1971
Seymour, 1979; Rand , 1968ft
Seymour, 1979
28-30°
27-30°
1980
1980
1980
1980
1980
Crocodilians
13.1
2.0
5.2
4.9
ADAPTATIONS TO UNDERGROUND NESTING
439
•u2
150
144
140
138
134
21
124
30
122
32
128
29
20
FIG. 1. The incubation mound of a Mallee Fowl (Leipoa ocellata) on 15 October 1979, approximately six
weeks after the first egg was laid. Gas tensions are presented at selected depths in the center of the mound.
Unpublished data were collected by Seymour, Vleck, and Vleck.
Despite the various sources of heat, me- ally accomplish this by constructing a new
gapode eggs are incubated at tempera- mound each breeding season while Mallee
tures surprisingly close to those of other Fowl often open previously used mounds
bird eggs (Table 1). Whereas reptile eggs and add fresh litter. Scrub Fowl may conare usually incubated at about 30°C (Ta- tinually add new material to the outside of
ble 2), incubation temperatures of five an old mound which causes the mounds to
megapode species average about 35.8°C grow through the years (Frith, 1956a).
(range = 31-39°C) (Frith, 1956a). In Brush
The rate of decomposition clearly deTurkey and Mallee Fowl mounds, the cen- pends on adequate moisture in the litter.
tral temperature is maintained remarkably The onset of egg laying in Mallee Fowl is
constant by the industrious activities of the delayed until the gathered material is sufmales which periodically dig down to the ficiently moistened by winter and spring
egg layer, test the temperature with the rains (Frith, 1956a). Breeding in Brush
head or beak and then open or close the Turkeys is also dependent on sufficient
mound as appropriate. Aside from regu- rain, and these birds are reported to form
lation by the birds, the large mass of many a funnel in the top of the mound prior to
mounds is important for thermal stability. rain so that the water soaks into it (Fleay,
Baltin (1969) estimated that a Brush Tur- 1937).
key mound consists of about 3.6 metric
Organic decomposition in megapode
tons of leaf litter and soil, a mixture with mounds is totally aerobic and occurs
good insulative properties.
through the action of microorganisms, resBirds that rely on organic heat for in- piration by the plant material itself and
cubation must incorporate fresh material spontaneous oxidation of organic material.
in a mound each year. Brush Turkeys usu- No location is anoxic (Seymour, Vleck, and
440
R. S. SEYMOUR AND R. A. ACKERMAN
Vleck, unpublished). Temperature increases with depth into the mound, and
Po2 and Pco2 depart from atmospheric
levels in a similar fashion (Fig. 1). This suggests that both heat and gas move through
the mound primarily by diffusion. The
correlation between gas tensions and temperature in Brush Turkey mounds led
Drent (1975) to wonder whether the bird
regulated temperature or gas tensions, but
experiments of Frith (1957) showed that
temperature is the stimulus in Mallee
Fowl.
Measurements have been made of O2
consumption and CO2 production by the
decomposing plant material in megapode
mounds, and we know the pattern of O2
consumption during embryonic development (Vleck, Vleck, and Seymour, unpublished). It is therefore possible to make an
assessment of the relative effects of egg
and mound metabolism on the gas tensions in the mound. The mean O2 consumption of a Brush Turkey egg throughout incubation is about 20 ml O2/hr. With
a 49 day incubation period and laying interval of 2-5 days (Baltin, 1969), there are
up to 20 eggs in the mound at once.
Therefore the total O2 consumption by the
eggs is about 400 ml O2/hr. This is about
3% of the O2 consumption (13.7 liters/hr)
by the mound itself. Hence mound metabolism appears to be the major determinant
of mound gases and temperature in the
Brush Turkey mound.
The eggs
Water loss and the aircell. Because Mallee
Fowl and Brush Turkey eggs are incubated in a gaseous environment that is virtually saturated with water vapor, the only
water loss occurs by virtue of small vapor
pressure differences across the shell that
develop as a consequence of the embryo's
heat production (Packard et al., 1977).
Mallee Fowl eggs, incubated in their own
mound material in the laboratory, lost only
about 2—3% of their original mass during
the course of development (Vleck, Vleck,
and Seymour, unpublished). As water is
lost, a small bubble appears beneath the
shell membranes and moves around in the
albumen, always remaining uppermost. In
this regard, it is distinct from the aircell
that forms in most bird eggs between the
inner and outer shell membranes and remains fixed at one end of the egg. An aircell is also lacking in the eggs of Brush
Turkeys (Baltin, 1969) and Scrub Fowl
(Meyer, 1930), but Baltin reported seeing small gas bubbles under the membranes
in even freshly laid eggs.
The aircell in most birds plays an important role in the slow transition from
chorioallantoic to pulmonary respiration
(Visschedijk, 1968). Because the small bubble under the membranes is insufficient to
permit pulmonary respiration within the
shell, the megapodes do not pip internally
and cannot breathe until the shell and
membranes are broken and the fluids are
drained from around the head. From the
moment this occurs, the chick requires
only 30 min or so to completely free itself
from the shell. During this time, breathing
is evident but we do not know the extent
of perfusion of the chorioallantois. However, the explosive nature of hatching suggests that perfusion is stopped much more
quickly in megapodes than in other birds.
Because rapid circulatory changes are well
known for mammals at birth, a rapid shift
in gas exchange organs is not surprising,
and we are forced to wonder why the transition takes so long in other birds.
Respiratory gas exchange. In eggs incubat-
ed above ground, there is a selective pressure on eggshell conductance and excessive evaporation is avoided. This selective
pressure is relaxed below ground where
humidity is nearly saturated. Here, in a
hypercapnic and hypoxic environment,
there appears to be selection for increased
shell conductance so that tissue gas concentrations are not intolerable (Table 1).
The extent of increase, moreover, is related to the deviation of the mound gases
from the free atmosphere. For example,
the Mallee Fowl shell conductance is about
35% higher than predicted (by egg mass
and incubation time) and the mound Pco2
reaches about 30 torr whereas the Brush
Turkey's conductance is about 120% above
predicted and the mound Pco 2 reaches
about 70 torr. The increased conductance
results from an abnormally thin shell; the
ADAPTATIONS TO UNDERGROUND NESTING
functional pore area is actually lower than
predicted by other bird eggs (Table 1).
Perhaps it is significant that conductance
is increased this way. A thin shell is not a
liability in the protective mound environment and it is an advantage to the adult,
because it reduces the energy and materials required for shell formation, and to
the hatchling, because it facilitates quick
emergence.
Energetics of the embryo. T h e failure of
megapode eggs to lose much water during
incubation may be connected with the energy budgets for the developing embryo.
Most bird eggs lose about 14-18% of their
mass by evaporation (Rahn and Ar, 1974;
Rahn et ai, 1976; Drent, 1970). This volume potentially represents an increased
energy store for megapode development.
The yolk of Scrub Fowl accounts for 67%
of the egg volume (Meyer, 1930). In
Brush Turkey eggs, it averages about 49%
of initial egg volume (Vleck, Vleck, and
Seymour, unpublished). Both of these values are higher than data from other precocial (35.2%) and altricial (19.8%) species
(Romanoff and Romanoff, 1949). These
energy stores could ultimately appear as a
heavier hatchling (relative to the fresh egg
weight) a high metabolic rate or a long development time. But hatchling Brush Turkeys weigh 64-70% of the fresh egg and
Mallee Fowl about 67.5% (Seymour, Vleck,
and Vleck, unpublished; Baltin, 1969); this
is about the same as the average of 68%
for many birds (Romanoff, 1944). Therefore it seems that the additional energy
supports the higher than predicted metabolism of the embryo during a long incubation period (Table 1). The result is an
extremely precocial hatchling which is capable of flight 24 hr after leaving the egg
(Frith, 1962).
The precocity of megapode chicks is also
related to the relatively large eggs. Adult
female Brush Turkeys and Mallee Fowl
weigh about 1800 g (Baltin, 1969; Frith,
1959) which, according to Lack's (1968)
data for the Galliformes, predicts a weight
of about 60 g in eggs laid every 1-2 days.
Brush Turkeys require about 2—5 days
(Baltin, 1969) and Mallee Fowl about 5-9
days (Frith, 1959) to produce eggs weigh-
441
ing about 200 and 170 g respectively.
Therefore the rate of egg tissue formation
appears similar among the Galliformes.
THE EGYPTIAN PLOVER
Besides megapodes, the Egyptian Plover
(Pluvianus aegyptius) is one of the few bird
species reported to bury their eggs (Howell, 1979). The adults lay 2-3 eggs of about
9 g each in shallow scrape nests in sandy
areas near rivers. The eggs are covered by
2-3 mm of sand during the day and the
adults incubate over the sand. At night the
eggs are uncovered and incubated in contact with the brood patch to maintain
about 38°C. During the day when ambient
temperatures may rise well above 40°C, the
adults soak their belly feathers in the nearby river and return to wet the sand surrounding the eggs. Evaporative cooling
keeps egg temperatures at 38-41°C.
The belly soaking behavior results in
high nest humidities and the eggs lose only
11% of their initial mass. This is slightly
lower than predicted for other birds (Rahn
and Ar, 1974) and occurs despite a longer
incubation period and greater eggshell gas
conductance than predicted from egg
mass (Rahn and Ar, 1974). The incubation
period of the Egyptian Plover is long and
may have the adaptive benefit of extreme
precocity at hatching. The fresh chick
weighs about 75% of initial egg mass which
is somewhat greater than that reported for
other birds (Romanoff, 1944).
Howell (1979) suggests that the initial
evolutionary advantage of egg burying was
concealment and that the combination of
burying and wetting behavior ultimately
permitted egg survival in what otherwise
would be a lethal environment.
REPTILES
The nests
Most reptiles deposit their eggs in the
ground or in litter at ground surface.
Small reptiles may scatter their egg clutches (1-2 eggs) in suitable sites in the ground
litter (Rand, 1967). Large reptiles, however, may bury their large clutches (10200 eggs) in holes excavated in the ground
(hole nesters) or in raised mounds (mound
nesters). These reptiles include all of the
442
R. S. SEYMOUR AND R. A. ACKERMAN
Hole nest temperatures are chiefly determined by the temperature of the nesting medium, which may influence the timing of egg laying (Rand, 1972). Egg
temperatures in the hole nest may rise
above the temperature of the nesting
beach (Hendrickson, 1958; Carr and
Hirth, 1961; Bustard, 1972) and a temperature gradient of this magnitude may
exist between the center and periphery of
the nest toward the end of incubation
(Bustard, 1972).
As in megapode mounds, temperatures
in crocodilian mound nests may be heated
by organic decomposition (Chabreck,
1973; Webb et ai, 1977; Goodwin and
Marion, 1978) but there are no measurements of mound metabolism. Neil (1971)
suggested
that, among mound building
10
6O
20
30
40
crocodilians, the prevention of egg overTIME (days)
heating is a major factor in the selection of
FIG. 2. Oxygen and carbon dioxide tensions in the nesting site. Perhaps in some cases, a
Green Turtle (Chelonin mydas) and Loggerhead Turtle mound is constructed for temperature sta(Caretta caretta) nests during incubation. Data are
summarized from Ackerman (1977) for three, 100 bility only and the heat production by deegg nests of each species. Hatching occurred near 60 composition in the mound may be a disdays for Chelonia and 50 days for Caretta. Curves advantage.
were drawn by eye.
The eggs
marine, and most of the semi-aquatic and
terrestrial turtles (Carr, 1952, 1967; Ernst
and Barbour, 1972), some larger lizards
(Hirth, 1963; Bartholomew, 1966; Rand,
1968a, 1972) and all the alligators and
crocodiles (Greer, 1970, 1971; Neil, 1971).
Hole nests may be shallow scrapes or laboriously constructed holes or tunnels
often in a sand substrate. The clutch is deposited, covered and left to develop. Crocodilians are probably the only reptilian
mound nesters but many species dig holes
(Greer, 1971). The mounds are constructed of soil and vegetation raised up to about
1 m above ground level, often in a shady
location (Neil, 1971). The egg clutch is deposited inside and completely covered with
material from the mound.
The temperatures of most clutches are
around 30°C (Table 2), but there may be
notable exceptions to this generalization.
For example, characteristic mound temperatures are in excess of 35°C for Crocodylus novaeguineae (Neil, 1971).
Thermal relations. There is very little information on the thermal requirements
for incubation of eggs of underground
nesters although there is more for other
reptiles. Some crocodile eggs do best
around 30°C (Bustard, 1971a). Sea turtle
eggs can be successfully incubated between
about 26°C and 35°C (Bustard, 19716), but
appear to have greatest hatching success
between 28°C and 32°C (Bustard and
Greenham, 1968; Simon, 1975).
Water exchange. In contrast with most
avian eggs which must lose water, many
reptilian eggs increase in mass during incubation by taking up water from the substrate.
However, water may be exchanged in
both directions by diffusion of water vapor
or by liquid flow (Tracy et at, 1978; Packard et ai, 1979a). This occurs through fibrous membranes or discrete pores in the
shell. Shell pores may occur in some hard
and soft shelled eggs but not in others
(Young, 1950; Packard and Packard,
1979; Sexton et ai, 1979). Hard shelled
ADAPTATIONS TO UNDERGROUND NESTING
443
alligator eggs do have pores (Packard et within the clutch. Ackerman (1977) sugal., 19796) while soft shelled sea turtle eggs gested that the characteristic nesting bedo not (Ackerman, unpublished). Consis- havior of sea turtles which resulted in the
tent with high nest humidity, the water va- interior of the egg clutch being free of
por conductance in reptilian eggs is gen- sand (Carr, 1967) was related to the gas
erally greater than predicted by most birds exchange requirements of the eggs. Simon
(Packard et al, 1979«, b\ Harrison et al., (1975) reported that sea turtle egg mor1978; Ackerman and Rahn, unpublished). tality increased when the spaces between
Typical values range from 2 to 60 times the eggs were filled with sand. This may
the avian predictions.
be due to impeded gas exchange by the
Respiratory gas exchange. T h e O 2 con- eggs (Ackerman, 1980).
sumption of reptilian eggs increases continuously through incubation (Clark, 1953;
DINOSAURS
Lynn and Von Brand, 1945; Dmi'el, 1970;
Prange and Ackerman, 1974) reaching its
Most values of shell gas conductance in
maximum level just prior to hatching. avian eggs have been obtained by measurOxygen uptake increases during hatching ing water loss with a known gradient of
and returns afterwards to prehatching water vapor pressure across the shell (Ar
levels (Lynn and Von Brand, 1945; Prange et al., 1974). Conductance can also be esand Ackerman, 1974). Although the val- timated by direct morphometric analysis of
ues for individual reptilian eggs are low the pore structure. In eggs with simple
compared to avian eggs (Seymour, 1979), straight pores such as hens' eggs, there is
the metabolic rate of a large clutch may be good correlation between the values obappreciable. Because most crocodilians tained by the gravimetric method and the
and sea turtles produce clutches ranging direct method (Wangensteen et al., 1970/
from 30 to 200 eggs and hatchlings range 71; Hoyt, et al., 1979). In several species
in mass from 10 to 60 g, the O2 consump- of fossil dinosaur eggs, the hard, caltion of these clutches can exceed 10 liters/ careous shell structure remains intact and
day. Sea turtle (Chelonia mydas, Caretta ca- reveals simple pores. Thus we can assess
retta) embryos consume about 5 ml O2/ shell gas conductance in animals which
g-day (Ackerman, 1975; Prange and Ack- have been extinct for over 65 million
erman, 1974) just prior to hatching. Near years (Seymour, 1979). Furthermore, the
hatching, a clutch of 100 Green Sea Turtle conductance may correlate with the hueggs producing 22 g hatchlings would con- midity in dinosaur nests and suggest somesume about 11 liters O2/day (Ackerman, thing about dinosaur incubation behavior.
1977). As in buried avian eggs, this high
Shell structure has been analyzed in
metabolic rate occurs in an environment three species of Upper Cretaceous dinowhich impedes the movement of gases. In saurs: a sauropod from southern France
the nests of the Green (Chelonia mydas) and (Hypselosaurus priscus), an unnamed sauroLoggerhead (Caretta caretta) Turtles, Po2 pod from the Gobi Desert and a small cerfalls to about 80-110 torr and Pco2 rises atopsian also from the Gobi (Protoceratops
to 30-50 torr during incubation (Fig. 2). andrewsi). The best data come from the
The description of gas exchange by sea 2100 g eggs of Hypselosaurus which show
turtle nests is simplified by the fact that a shell conductance over seven times
there is little or no metabolism occurring higher than predicted by similarly sized
in the surrounding sand and by the spher- bird eggs. Protoceratops eggs (360 g) are
ical symmetry of the nest gas exchange over 4 times, and the "multi-canalicular"
process (Ackerman, 1977). This process is eggs (1800 g) of the Gobi sauropod are
sensitive to such physical parameters as the over 100 times higher. This is evidence
grain size and water content of the sand that the eggs were incubated in high huwhich varies from beach to beach. Gradi- midity environments, possibly underents in gas tension develop not only be- ground or in incubation mounds. It is clear
tween the egg clutch and beach but also that the conditions in many living birds'
444
R. S. SEYMOUR AND R. A. ACKERMAN
so high that the differences in O2 tension
across them would have been less than 2
torr (Seymour, 1979). Thus the conductance of the matrix surrounding a buried
clutch is of primary importance in determining the gas tensions inside the eggshell.
Another important factor determining
gas tensions in the nest is the metabolic
rate of the eggs. It is possible for a buried
nest to be so large that in late development, diffusion would fail to supply the
gas exchange requirements of the embryos. Ackerman (1975, 1980) proposed
FIG. 3. Calculated maximum rates of oxygen con- that the requirement for optimal gas tensumption of entire clutches of buried eggs shortly sions in the nest might limit clutch size in
before hatching. The least squares regression line is
based on the data from turtles and crocodilians only. marine turtles and account for i) the reThe data are from Seymour (1979) and Ackerman markable selectivity of the females for cer(1980) except for the megapode data which are de- tain nesting beaches with suitable gas
rived from unpublished work of Vleck, Vleck, and transport properties, ii) the similarity of
Seymour.
clutch mass between species of very different body weights, and iii) the requirement
for multiple layings within a year. He
nests (Table 1) would have fatally dehy- found that the gaseous environment of
drated the dinosaur embryos if their tol- natural nests resulted in the shortest inerances to water loss and their incubation cubation time and greatest hatching suctimes were at all similar to modern birds cess of Chelonia mydas and Caretta caretta.
and reptiles (Seymour, 1979). The fossil Deviations from this optimum, as would
sites of Protoceratops show that the clutches occur if more or fewer eggs were deposwere deposited in three layers, with the ited in a nest, resulted in longer incubation
eggs separated by sand (Brown and time and poorer hatch, both results being
Schlaikjer, 1940), a conformation indicat- evolutionarily disadvantageous. This is
ing hole nesting. Fossil nests of Hypselosau- reason to believe that the maximum metrus, on the other hand, suggest that an in- abolic rate of a buried sea turtle clutch is
cubation mound was constructed. There is less than about 800 ml O2/hr. The Po2
evidence that the adult did not excavate a would be about 100 torr and the Pco2
hole, and the clutches are associated with about 40 torr in the center of a nest mefossilized rushes similar to those incorpo- tabolising at that rate in clean beach sand
rated into some crocodilian mounds (Ackerman, 1977).
(Dughi and Sirugue, 1966).
Nest gas tensions will be more extreme
if decomposing material is incorporated
LIMITS ON CLUTCH SIZE
around the eggs. It is therefore significant
Gas transfer between the atmosphere that the largest clutch mass (13.1 kg, Table
and a clutch of buried eggs occurs by dif- 2) with a calculated maximum O2 confusion through the soil or mound material. sumption of 775 ml O2/hr (Seymour, 1979)
The rate of diffusion depends on gas pres- occurs in Crocodylus niloticus which does
sure gradients developed by egg metabo- not include organic material in its hole nest
lism and organic decomposition in the soil. (Cott, 1961). Crocodylus porosus, on the othThe increased shell conductance in buried er hand, is a similarly sized animal but it
eggs may be viewed as an adaptive com- incubates its eggs in a mound of almost
pensation for the soil's resistance to dif- pure vegetation (Webb et ah, 1977). This
fusion. Nevertheless, there is a limit to this behavior may limit its clutch size to 5.6 kg
compensation and the limit is evident in with a calculated O, consumption of only
dinosaur eggshells that have conductances 395 ml O.,/hr.
Cetalopsian
ADULT
BODY
Dinosaui
WEIGHT
<Kg>
ADAPTATIONS TO UNDERGROUND NESTING
Of course, small reptiles cannot lay very
large clutches, so we would expect to see
a limit on clutch mass only in large reptiles.
Indeed, the limit becomes obvious only if
we include the data from the largest living
reptiles and dinosaurs (Fig. 3). Not only do
dinosaur fossils provide eggshell morphology, but three species also indicate egg
weight and clutch size. Whereas the clutch
represents 1-10% of the adult body weight
in living large reptiles, it is only 0.1% in
the 10 ton sauropod, Hypselosaurus (Seymour, 1979). With an allometric relationship between egg weight and maximum
egg metabolism in reptiles as a guide, Seymour (1979) calculates that the clutch O2
consumption reached only 300-400 ml O2/
hr, a value similar to those of living reptile
clutches. Had this sauropod's clutch conformed to a prediction based on adult
weight (Fig. 3), there would have been
about 116 eggs totalling about 250 kg. The
clutch would have consumed 7500 ml O2/
hr and reduced the Po2 in the center of
the egg mass to zero. However, there is
little doubt that the fossil sites of these sauropods contain complete clutches of 4-6
eggs totalling only 10 kg (Dughi and Sirugue, 1966).
Is it possible that the nest environment
severely restricted the reproductive effort
of dinosaurs? The fossil beds in southern
France suggest not. They provide evidence
that a single female sauropod, Hypselosaurus, actually divided up her eggs into separate clutches. The clutches were evenly
spaced in up to five parallel lines, each line
containing 15-20 eggs. A total of about 50
eggs was deposited—a reasonable reproductive effort for a 10-ton reptile. The
considerations of gas exchange in the nest
provide a plausible explanation for the necessity of this dinosaur's behavior.
The Brush Turkey has an alternate solution to the problem of clutch size. Because the mound can contain 20 eggs
which consume O2 at a total rate of about
400 ml O2/hr, and the mound consumes
O2 at about 30 times this rate, the nest gas
tensions tend to become extreme (Table
1). Were it not for the continual attention
of the male bird, which regularly turns
over the mound material and constructs
445
tunnels down to the egg level, it is doubtful
whether the eggs would survive either the
buildup of heat or the severe gaseous environment that could develop in the
mound (Baltin, 1969). It appears, therefore, that these underground nesters cansurvive total nest metabolic rates considerably above the suggested limit of 800 ml
O2/hr, but the survival depends on behavioral control of the mound environment.
ACKNOWLEDGMENTS
We thank C. M. Vleck and D. Vleck for
helping to collect new data on megapode
respiration and commenting on the manuscript. We appreciate the assistance of J.
Price, R. Altmann, P. Kempster and J.
Thompson in preparation of the manuscript and figures. This work was supported by the Australian Research Grants
Committee (RSS), an NSF grant, PCM7905052 (RAA), and an NSF grant,
DEB7903847 to the American Society of
Zoologists.
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