AMER. ZOOL., 25:999-1008 (1985)
Interrelations Among Water and Energy Relations of
Reptilian Eggs, Embryos, and Hatchlings1
C. RICHARD TRACY AND HOWARD L. SNELL2
Department of Zoology, Colorado State University,
Fort Collins, Colorado 80523
SYNOPSIS. Reptilian eggs previously categorized with respect to the flexibility of eggshells
appear to fall into two groups: endohydric eggs are those that are invested, by the female
parent at the time of oviposition, with all of the water necessary to complete embryogenesis;
and ectohydric eggs which need to absorb water from the nest medium to complete embryogenesis. Eggs of the Galapagos land iguana are unusual among most lepidosaurians by
having very permeable parchment shells, but containing a large albumen (apparently
serving as a reservoir of water for the embryo). It appears that the eggs of Galapagos land
iguanas can exploit an endohydric habit without the rigid, impermeable shell seen in other
endohydric eggs. This ability appears to be mediated by two factors: eggs of Galapagos
land iguanas are laid in dry soils which are essentially impermeable to water, and the very
large eggs of land iguanas have a relatively small surface area to volume ratio which results
in a relatively small exchange of water across the eggshell. It appears too that the water
relations of Galapagos land iguana eggs will affect the energetics of both the contained
embryo and the subsequent hatchling. Without adequate water, land iguana eggs will
produce hatchlings that are both smaller and possess less fat to sustain the juvenile during
the first year of life.
(Packard and Packard, 1980): (a) parchRapidly accumulating knowledge about ment-shell eggs of most lepidosaurians
the biology of vertebrate eggs (Rahn and characterized as differing". . . only slightly
Ar, 1974; Ar et al., 1974; Packard et al., from the presumed ancestral form," (b) pli1977; Packard and Packard, 1980; Tracy, able-shell eggs of many turtles character1982) has resulted in hypotheses about the ized as ". . . intermediate between the preevolution of terrestrial vertebrate eggs sumed ancestral condition and that of eggs
(Packard and Packard, 1980; Tracy, 1982). of contemporary birds," and (c) rigidIn this paper, we bring new data to bear shelled eggs of other turtles and crocodilupon (a) the question of the selective forces ians characterized as being similar to birds.
important to the evolution of different rep- This hypothetical phylogenetic sequence
tilian eggs, (b) reproductive adaptations in from eggs like those of lizards to eggs like
gravid female lizards with respect to the those of birds is seen to be a series of adapresulting environments of their incubating tations to avoid predation on eggs by
eggs, and (c) the interrelationships between arthropods and microbes. Specifically,
water relations of lizards as embryos and thickening of the eggshell is proposed to
be the major trend in reptilian eggs, and
their energetics as neonates.
other differences are seen to coevolve with
a thicker eggshell (Packard and Packard,
1980).
OVERVIEW OF EGG CHARACTERISTICS
One problem arising from the scenario
Reptilian eggs have been subdivided into
three categories proposed as a phyloge- presented above is that the "presumed
netic sequence between the ancestral rep- ancestral form" of the reptilian egg is reptilian egg and the egg found in birds today resented today only by reptilian groups
(lepidosaurians) arising very late in the history of reptiles (Romer, 1959). Is the pres1
From the Symposium on Animal Energetics: ent egg type of most lepidosaurians repAmphibians, Reptiles, and Birds presented at the Annual resentative of a primitive reptilian egg, or
Meeting of the American Society of Zoologists, 27- is it actually a highly evolved form of egg?
30 December 1983, at Philadelphia, Pennsylvania.
1
Reptilian eggs with different eggshells
Present address: Department of Biology, Memphis State University, Memphis, Tennessee 38152.
differ dramatically in water exchange with
INTRODUCTION
999
1000
C. R. T R A C Y A N D H. L. SNELL
200
180
160
co
O
0.
Ctotmphytut collmrlt •
140
Alllgmtor mlstlulppltnllt
•
Carmttm c«r«ff« *
CO
CO
<
o
o
120
100
UJ
80
60
'nest = - 2 0 0 kPa
40
20
40
60
80
100
% OF INCUBATION PERIOD
FIG. 1. Percent change in mass of eggs from three
species of reptiles. For each species there are two
lines. The upper line depicts the change in mass for
eggs buried with one half of their surface in contact
with vermiculite, and the lower line shows the change
in mass for eggs suspended above the vermiculite which
had a water potential of —200 kPa. All lines are fitted
by eye through the means of no less than three mean
masses of eggs weighed no less than six times during
the incubation period. Thus, each line was fitted
through 18-60 data points. The isolated symbols represent the mean masses of hatchlings incubated in
both experimental conditions. All methods are as in
Tracy et al. (1978).
their environments (Fig. 1). Parchmentshelled eggs can absorb proportionately
massive amounts of water from wet nest
media (Fig. 1), but if they absorb too much
water, they suffer high rates of mortality
(Tracy, 1980; W. H. N. Gutzke, personal
communication; Tracy and Snell, in preparation; see also Fig. 4). These eggs also
have the capacity to lose water at rapid
rates (Fig. 1), and will desiccate quickly
causing the death of the contained embryo
(Tracy, 1980; Packard, 1980; W. H. N.
Gutzke, personal communication; Tracy
and Snell, in preparation; see also Fig. 4).
The amount of albumen in parchmentshelled eggs is generally almost nonexistent (Table 1). Egg albumen can function in two ways: (1) as a reservoir of water
for the developing embryo (the albumen
is approximately 98% water in reptilian
eggs; Tracy, unpublished data), and (2) the
albumen is a barrier to the invasion of the
egg by microbes (Movchan and Gabaeva,
1967; Ewert, 1979). Why then would a lepidosaurian produce an egg without these
seemingly beneficial properties? Does such
an egg lack these properties because it is
simply primitive? Tracy (1980, 1982) has
suggested three situations that would select
for a parchment-shelled egg: (a) environments in which water is relatively scarce
for gravid females (environments such as
arid deserts), but available (in the form of
soil moisture) to be absorbed by permeable
eggs; (b) environments in which a reduced
bulk of individual eggs would be favored
(either because bulky eggs could make
females more vulnerable to predation
[Shine, 1980], or because bulky eggs force
a relatively small clutch); and (c) in environments that favor large hatchlings (the
size of the yolk ultimately determines the
size of the hatchling provided that all of
the yolk is metabolized, so an egg containing only yolk can produce the largest
hatchling per unit mass of egg).
It appears that parchment-shelled eggs
represent an evolutionary strategy that
could evolve in response to several selective forces, but it is a strategy requiring
that eggs absorb water from outside of the
egg (a) to complete embryogenesis (Packard** al., 1977; Tracy, 1980; Andrews and
Sexton, 1981), or (b) to produce hatchlings
of maximum body mass (Packard et al.,
1980; and see Fig. 2). Thus, we can call
this phenotype an "ectohydric" egg defined
as an egg not invested, at the time of oviposition, with all of the water necessary
fully to complete embryogenesis.
Pliable-shelled eggs do not generally
exchange water nearly as rapidly as parchment-shelled eggs (see Fig. 1 for example),
and many such eggs appear to have more
albumen than do the parchment-shelled
eggs of most small lizards (Table 1). Rigidshelled eggs are resistant to rapid flux of
WATER-ENERGY RELATIONS OF REPTILIAN YOUNG
1001
TABLE 1. Mass of albumen in eggs as a percent of the total mass of the egg at the time of oviposition.
Species
% Albumen
F
-gg '
Lizards
Coleonyx variegatus
Sceloporus graciosus
Dipsosaurus dorsalis
Holbrookia texana
Sceloporus undulatus
Sceloporus graciosus
Uta slansburiana
Urosaurus ornatus
Phrynosoma cornutum
Anolis carolinensis
Cnemidophorus exanguis
Amblyrhynchus cristatus
Conolophus subcrulatus
4
3
3
19
28
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
Parchment-shelled
34
37
41
Pliable-shelled
Pliable-shelled
Pliable-shelled
44
Rigid-shelled
60
Rigid-shelled
2
1
2
4
2
4
3
7
Turtles
Chrysemys picta
Chrysemys concinna
Caretta caretta
Crocodilians
Alligator mississippiensis
Birds
Gallus domesticus
water across the eggshell (Fig. 1), and
appear to have the greatest amount of
albumen at oviposition (Table 1). Eggs that
are relatively impermeable to water certainly would have to contain enough water
(Packard and Packard, 1980), usually in the
form of albumen (Tracy, 1982), to complete embryogenesis. The combined characteristics of a relatively impermeable eggshell and a large albumen may represent
an evolutionary strategy to resist invasion
by predators and/or microbes (Packard and
Packard, 1980; Tracy, 1982), or to resist
lethal rates of exchanges of water (rates
that could desiccate or "drown" the
embryo; Tracy, 1980, 1982). Some pliableshelled eggs and rigid-shelled eggs apparently contain enough albumen that
exchanges of water (into or out of the egg)
do not influence the size of the hatchling
(Packard et al, 1979; and see Fig. 2). Thus,
this phenotype can be called an "endohydric" egg denned as an egg invested, at the
time of oviposition, with all of the water
necessary to complete embryogenesis.
These patterns of adaptation in eggs suggest that the component parts of eggs may
evolve somewhat independently (Tracy,
1982). For example, it appears that the size
of the yolk may reflect selective forces on
the size of the hatchling, because the size
of yolk determines the upper limit of the
size of the hatchling (Tracy, 1982).
Whereas the eggshell and albumen may
coevolve in response to predators and/or
pathogenic microorganisms on the contents of the egg (Packard and Packard,
1980), and/or to hydric environments that
are too dry (potentially causing desiccation) or too wet (causing "drowning") for
the successful incubation of the egg (Tracy,
1980, 1982).
WATER RELATIONS OF CONOLOPHUS
Introduction
The dichotomous classification of eggs
as "ectohydric" or "endohydric," and the
hypothesis that the components of eggs may
evolve independently, allow general predictions about the kind of eggs one would
expect among reptiles in different environments. For example, Galapagos land
iguanas commonly lay eggs in very dry
environments (Christian, unpublished data;
Snell and Tracy, 1985). If the eggs are
1002
C. R. TRACY AND H. L. SNELL
were centrifuged using a hand sling, and
then carefully opened to remove albumen
into a cup. After all of the albumen was
O
/
- 1.00 o
removed, and its mass determined, the
masses of yolk and eggshell were measured
separately. (All masses were measured to
.
c
the nearest 0.01 g with an O'Haus "Dialo
^
a-Gram" balance.) These masses were then
Trionyx
normalized to the original mass of the egg
jSSXi-^——
Alllgttor
.
"
to compare with data for other eggs (Table
Cartm
- 0.50 O
1).
Forty eggs were placed in plastic-lined
wooden boxes filled with soil previously
mixed with water to provide one of four
-10
-8
-6
-4
-2
0
different soil-water potentials (0, —250,
INCUBATION WATER POTENTIAL I M P i l
-7,500, and <-10,000 kPa). Eggs were
FIG. 2. Mass of hatchlings, as a percent of the mass placed in the soil so that either 25% or 75%
of their eggs at oviposition, in relation to the water of their surface area was exposed to the
potential of laboratory nest medium. Data for Chel- substrate. The treatment boxes were placed
ydra, Chrysemys, Trionyx, and Callisaurus were taken
from Packard <?< a/., 1980; Packard et al., 1981; Pack- in a large box that was buried in an "artiard <?< a/., 1980; and Packard etai, 1980, respectively. ficial burrow" so that the eggs within the
Data for Sceloporus (T) and (C) were for Sceloporusbox would be ca. 0.3 m below the surface
undulatus from northwestern Texas and west central of the ground (approximately the mean
Colorado respectively (Tracy, unpublished). Data for depth of land iguana nest burrows on Isla
Alligator mississippiensis were from eggs taken from
west coastal Louisiana, and data for Caretta caretta Plaza Sur; Snell and Snell, unpublished). A
from eggs collected from the west central coast of thermocouple was placed in the large box
Florida (Tracy, unpublished). All eggs were incubated to monitor the incubation temperature.
on vermiculite according to the methods of Tracy et
Periodically, the incubation box was
al. (1978).
excavated, the eggs weighed to within 0.02
g, and the treatment boxes recalibrated to
indeed laid in nests that are dry enough the desired water potential by adding any
that water can not be absorbed by the egg, water lost during incubation. The moisit would seem reasonable to predict that ture of incubation substrates was deterthe eggs should be endohydric. However, mined by measuring the gas emanation
endohydric eggs are usually less permeable from a mixture of a measured amount of
than the parchment-shelled eggs of most wet soil with an excess of calcium carbide
lizards. Thus, we wondered if Galapagos (measurements were made to 0.1% moisland iguanas would (a) have eggs different ture relative to the dry mass of soil using
from the endohydric eggs predicted for a Speedy Moisture Tester). The relationthem, or (b) behaviorally select nest sites ship between soil moisture and water
in rare patches of moist soil in which parch- potential for the incubation soil was later
ment-shelled, ectohydric eggs could absorb determined in the laboratory using a Weswater.
cor C-52 psychrometer to measure water
potential. The incubation boxes were excaMaterials and methods
vated every 3-4 days during the first 20
Eggs of the Galapagos land iguanas of days of incubation, every 10 days during
Isla Plaza Sur were studied in 1981. De- the middle of the incubation period, and
tailed characteristics of this population of every day during the last 10 days of the
lizards can be found in Snell et al. (1984). incubation period (frequent excavations
Gravid females constructing nest burrows near the end of the incubation period were
were checked daily until they laid their necessary to recover hatchlings on the day
eggs. Then a sample of nest burrows were of hatching). Incubation temperatures
excavated and the eggs removed. Four eggs remained relatively constant at ca. 30° ±
—
•
WATER-ENERGY RELATIONS OF REPTILIAN YOUNG
2°C throughout essentially all of the incubation period.
Hatchlings were removed from the incubation boxes within less than one day of
hatching, and their mass and length were
measured.
1003
CONOLOPHUS
Or.Po.3/4 buried
250 hPa, 3/4 buried
OkPa, 1/4 buried
-25OkPo, 1/4 buried
•7.500 hPo, 3/4 buried
'-7.500r.Pa, 1/4 buried
Results and interpretations
Eggs exposed to water potentials of 0
and —250 kPa absorbed water regardless
DAYS OF INCUBATION
of the amount of surface area exposed to
the soil; however, eggs with a greater FIG. 3. Mass of eggs, as a percent of their mass at
during the course of incubation on nest
amount of their area exposed to the soil oviposition,
medium differing in water potential. Lines were fit
absorbed water at a greater rate (Fig. 3). by eye through data on forty eggs, evenly divided
This is consistent with the model which among treatments, and reweighed up to twenty times
assumes that the principal source of each during incubation. Thus, each line was fit through
absorbed water is liquid water transferred data on 20-120 weighings of eggs. See text for details
from the interstices of the substrate (Pack- of experiments.
ard et al., 1977; Tracy, 1980, 1982). Eggs
exposed to drier soils lost water (Fig. 3), relationship between rate of water uptake
and eggs exposed to very dry soil vs. substrate water potential to a point to
(<-10,000 kPa) became lethally desic- which there is no exchange of water, that
cated by day 20 of the incubation period point should be where the water potential
after losing ca. 30% of their original mass of the substrate exactly equals the water
(Fig. 3). Eggs that absorbed water, never- potential of the eggs. For the land iguanas,
theless, did not absorb relative quantities this interpolation indicates that the water
as great as those absorbed by the eggs of potential of the eggs was ca. —750 kPa (Fig.
some small iguanid lizards (see Fig. 1; and 5) which is similar to water potentials meaTracy, 1980). This could be the result of sured for several species of temperate
several characteristics of land iguana eggs: iguanids (Tracy et al., in preparation). Thus,
(a) the eggshells could be less conductive, it appears that the proportionately small
and thus slow the rate of absorption (this rates of relative water uptake by land iguana
possible mechanism was not evaluated by eggs is not due to a lower water potential
us); (b) the surface area relative to the vol- of the egg contents.
ume of land iguana eggs is much less than
Eggs incubated on substrates of both low
that of a smaller egg, and therefore, the and high water potential suffered the highrelative volume of water absorbed through est rates of mortality among the eggs in
the eggshell surface should be less if the our experiments (Fig. 4). This pattern is
eggshell is not more porous (this mecha- essentially identical to that of other lizards
nism must play a role in the disparate rates and snakes (Tracy, 1980; Tracy and Snell,
of relative water uptake); and (c) the water in preparation; W. H. N. Gutzke, personal
potential of the contents of land iguana communication). However, eggs living long
eggs could be less than that of smaller eggs, enough to hatch produced hatchlings
and therefore, force slower rates of water whose sizes (mass and length) were signifabsorption (this mechanism is evaluated icantly correlated with substrate water
below).
potential (Fig. 4). This pattern is identical
Measurements of the rate of water to that found in Galapagos marine iguanas
exchange in the first 10 days of incubation (Tracy and Snell, in preparation), and simfor eggs buried to different degrees, and ilar to that found in several species of lizfor eggs exposed to soils of different water ards and turtles (Fig. 2). Furthermore, the
potentials, allow an interpolative analysis masses of the hatchlings relative to the
of the water potential of the eggs at ovi- masses of the eggs (Fig. 4) are more similar
position. Specifically, if one interpolates the to those of alligators and turtles than to
1004
C. R. TRACY AND H. L. SNELL
CojMtopftu* subcriMftus
PLAZA SUR,
GALAPAGOS
CONOLOPHUS
3/4 buried
eggs
•o
0.5
LJ
CD
<
X
LJ
LU
I
o
LU
FIG. 4. Survivorship of embryos through the first 50
days of incubation, and size of hatchlings as functions
of the water potential of the incubation medium. All
patterns are statistically significant (chi-square contingency table test of survivorship, and AOV on the
regression of relative mass and relative length of
hatchlings on water potential of nest medium).
-0.5
-1000
those of small lizards (Fig. 2). Finally, the
amount of albumen found in the eggs of
land iguanas (at the time of oviposition) is
remarkably high (28%) relative to that of
other lizards (Table 1).
Conclusions
Eggs of Galapagos land iguanas appear
to have several properties similar to those
of endohydric eggs: large size, proportionately large albumen, and relatively slow
rates of water uptake. Nevertheless, these
eggs are similar to ectohydric eggs in being
able to lose water rapidly enough to become
lethally desiccated. Furthermore, we know
from other data (see Snell and Tracy, this
volume) that many nests in 1981 were dry
enough to cause lethal desiccation under
the artificial conditions of our study. How
then were the eggs able to survive the
seemingly desiccating conditions of the
natural nests? Perhaps we have been too
myopic in attributing all of the explanation
for rates of water exchange to the properties of the eggs and their eggshells?
We predicted earlier (Packard et al.,
1977) that liquid water transport to (or
from) eggs through very dry soil will be
controlled not just by the hydraulic con-
-1.0
-500
SOIL WATER POTENTIAL {kPa)
FIG. 5. Relative rates of uptake of water by eggs with
'A and 'A of their surfaces in contact with the substrate
having water potentials of 0 and —250 kPa. Lines
running through the mean rates for eggs buried at
different depths intersect at a point where the eggs
are predicted not to exchange water with the substrate at a water potential of —750 kPa.
ductance of the eggshell, but also by the
hydraulic properties of the soil which are
remarkably nonconductive when dry
(Tracy, 1976). Perhaps very large eggs can,
by virtue of their small surface area to volume ratio, exploit an endohydric habit by
(a) possessing a large reservoir of water in
the form of a large albumen; and (b) being
laid in very dry soil where water will be
lost, but not so rapidly that the enclosed
embryo will become lethally desiccated. If
this is the case, why did our "laboratory"
experiments on water exchange of eggs
show that eggs exposed to dry soils lost
water very rapidly? The answer to this
question is likely to be found in the fact
that we purposely disturbed the developing gradient of moisture beneath each egg
when we stirred the soil to recalibrate water
potential. This allowed us to correctly
WATER-ENERGY RELATIONS OF REPTILIAN YOUNG
report that the soil moistures next to the
experimental eggs were as we forced them
to be. However, in dry natural nests, the
water would be unable to move from the
egg (due to the low transport properties of
dry soils), and the egg would witness a
moister environment immediately adjacent to the eggshell. Such a phenomenon
has been measured in laboratory experiments with eggs of snapping turtles (W. H.
N. Gutzke, personal communication).
MODELLED WATER RELATIONS OF EGGS
IN DRY SOILS
1005
and me, were 9.47 x 10~6 kg/(m 2 • sec) and
1.81 x 10~6 kg/(m2 • sec) respectively. From
the calculated value of m% it was possible to
calculate the hydraulic conductance of the
eggs to water exchange between the substrate and the egg from the equation:
K = mJAbX
(3)
where K is the hydraulic conductance calculated to be 1.26 x 10-11sec/m,A1J'(kPa)
is the water potential difference between
the soil and the egg contents, and A is the
surface area across which liquid water is
transported which is calculated by the
equation from Hoyt (1976):
To assess the relationship between egg
size and the exchange of water by eggs in
(4)
A = [4.393 + 0.394 £]V0667
soils that establish a time-dependent gradient of moisture beneath the egg (or clutch where E is the elongation of the egg defined
of eggs), we performed a model simulation as the length/breadth of the egg (taken to
of water exchanges of eggs differing in size be 1.8 for the simulations here—approxas a function of the water potential of the imately the mean for all three species simsubstrate. We used the models of water ulated), and V is the volume of the egg
exchange from the literature (eqs. El, E2 approximated as the mass-density of the
and 11 of Tracy, 1982) to predict the rate egg (where density is approximately 1.01;
of water exchange for three sizes of lizard Hoyt, 1976).
eggs roughly equivalent to (a) Sceloporus The equations (Tracy, 1982) used to
undulatus (0.5 g), (b) Conolophus subcristatus evaluate the water balance of the eggs dif(50 g), and (c) Amblyrhynchus cristatus (100 fering in size also required data on the
g). We assumed that all modelled eggs had hydraulic conductivity and diffusivity of the
the same water potential (—750 kPa), and soil (Tracy, 1976). Simulations from these
the same hydraulic conductance. The rates equations and calculated parameters sugof exchange of water between the eggs and gest that eggs of all sizes should not
soil, and between the eggs and the atmo- exchange water with the soil when the
sphere of the nest chamber during the first water potential of the soil is below approx10 days of incubation, were calculated from imately — 500 kPa (Fig. 6). This is due to
the simultaneous solutions of the water the impermeability of undisturbed, dry soils
budgets of Conolophus eggs with 0.75 of (Tracy, 1976). Simulated water uptakes of
their surface in contact with the soil (at 0 eggs differing in size suggest that very small
kPa)
eggs have a capacity to absorb proportionately very large amounts of water, whereas
0.75m5 + 0.25m. = mt,
(1) larger and larger eggs have a diminishing
and eggs with 0.25 of their surface in con- capacity to absorb proportionately large
quantities of water. This does not mean
tact with the soil
that large eggs do not absorb a lot of water,
0.25m5 + 0.75me = mt.
(2) but it does mean that the amount of water
Here ms is the rate of water exchange absorbed is not a large fraction of the mass
between the egg and the substrate,' mc is of the eggs. The differences seen among
the rate of water vapor exchange between eggs of different sizes are due to the difthe egg and the atmosphere. ml for eq. 1 ferences in surface area relative to volume
and eq. 2 was taken from the data pre- of the eggs. Specifically, small eggs have a
sented in Figure 5 to be 7.55 x 10"6 and very large surface area relative to their vol3.77 x 10"6 kg/(m 2 sec) respectively, and ume, whereas the largest eggs have a much
the calculated rates of water exchange, ms diminished surface area to volume ratio.
1006
C. R. TRACY AND H. L. SNELL
EGGS TOTALLY BURIED IN SOIL
O.59
SO9
10
SCELOPORUS
CONOLOPHUS-
adaptations (evolutionary "strategy") promoting survival of eggs appears to include
(among other things) the size of the egg as
well as the morphological characteristics of
the shell and the amount of albumen. However, it also includes the selection of a nest
< environment that is either moist (allowing
O
X
the absorption of water), or very dry (preUJ
a: venting rapid losses of water).
UJ
100 9
-.O 5
I
AMBLYRHYNCHUS
-I04
-I0 1
-10*
SOIL WATER POTENTIAL tkPo)
-2
FIG. 6. Simulated water exchanges of eggs, differing
in size, as a function of the water potential of the
environment. See text for details of equations used
in the simulations.
In general, then, it appears that very
small eggs have the capacity to exploit an
ectohydric habit in which proportionately
large volumes of water can be taken from
the moist nest environment. Large eggs,
on the other hand, seem unable to absorb
relatively large quantities of water from
the environment, and thus might not be
able to exploit an ectohydric habit. These
simulations help to explain the paradox of
Galapagos iguana eggs wherein the eggs
have some properties normally associated
with ectohydric eggs {e.g., thin eggshell,
ability to absorb water, and the potential
to become dehydrated under artificial laboratory conditions), but also have some
properties normally associated with endohydric eggs {e.g., a relatively large albumen, and they are often laid in very dry
nests). Indeed, perhaps the large size of
iguana eggs is an adaptation to environments in which moisture is not predictably
available. Large eggs can absorb water, but
not relatively great quantities. However,
large eggs can contain large amounts of
albumen which can provide water to support embryogenesis. The combined effects
of a small surface to volume ratio, and the
impermeability of dry soils, allow large eggs
to survive in very dry nest environments
even though the eggs do not have a relatively impermeable shell such as that in
crocodilian eggs. Thus, the entire suite of
WATER-ENERGY INTERACTIONS
Eggs often possess a store of water in the
form of albumen, and hatchlings have
energy stores in the form of yolk and fat
(Snell and Tracy, 1985). Conversion of yolk
into fat must, due to the second law of
thermodynamics, cost some energy. Thus,
it would appear that conversion of yolk to
fat must carry some higher dividends than
those possible by simply using yolk as the
only store of energy for hatchlings. We have
speculated that fat should be used as a store
of energy for hatchlings that emerge from
their natal nests to an environment depauperate in energy resources (Snell and Tracy,
1985). However, what proximate processes mitigate against this adaptation? In
ectohydric eggs, water absorbed appears to
permit the metabolism of yolk into hatchling (Tracy, 1982). Thus, up to some limit,
the more water absorbed (or present in the
form of albumen), the bigger will be the
resulting hatchling. This is reminiscent of
a chemical equation suggesting that
yolk + water = hatchling. However, if
conversion of yolk into fat obeys the same
pseudochemical equation, then yolk +
water = hatchling + fat. Thus, a shortage
of water for the egg could cause either (or
both) a small hatchling (due to an incompletely converted yolk into hatchling), or
a hatchling with a relatively small amount
of fat (due to a yolk incompletely converted
into fat). This shortage of water for an egg
could, therefore, cause a potential reduction in survival of the resulting hatchling
in two ways: (a) by producing a hatchling
that is small (see Fox, 1978; and Ferguson
and Bohlen, 1983, for evidence that small
hatchlings can have reduced fitness in
iguanid lizards), and (b) by producing a
hatchling with a relatively small energy
store in the form of fat. In the latter case,
WATER-ENERGY RELATIONS OF REPTILIAN YOUNG
the water relations of the egg can affect
the energetic relations of the subsequent
hatchling.
OVERALL CONCLUSIONS
Adaptations for the hydric environment
of reptilian eggs have more dimensions than
previously imagined. Morphological adaptations of the eggs (especially the permeability of the eggshell, and the amount of
albumen) interact with behavioral adaptations of females in the selection of nest
sites that are either moist enough to allow
absorption of water by eggs, or are dry
enough to be impermeable to moisture
leaving the egg. Adaptations in eggs seem
roughly to separate into two catagories that
we have labelled "ectohydric" and
"endohydric," which identify the source of
water required for successful embryogenesis. It appears that egg size can constrain
water transport processes in eggs, so that
large eggs behave as endohydric eggs irrespective of eggshell properties. Finally, the
water relations of an egg appear to interact
complexly with the energy relations of the
embryo and subsequent hatchling. Thus,
water relations of eggs can represent a critical environmental interaction for reptilian
species.
In spite of the apparent pivotal importance of the egg stage in the life history of
some reptiles, a disturbingly sparse literature exists on the ecology of reptilian eggs,
and/or the evolutionary adaptations of
eggs, embryos, and hatchlings, Indeed, two
major reviews of the ecology of lizards
appeared within the last year (Burghardt
and Rand, 1982; and Huey et al., 1983),
and not even one page was devoted to the
ecology of lizard eggs. If the fitness of an
individual is defined in terms of the effectiveness of adaptations at all life-history
stages, then our literature is woefully
depauperate in the information necessary
to predict the fitness of reptiles.
ACKNOWLEDGMENTS
We wish to thank the Parque Nacional
Galapagos and the Charles Darwin
Research Station for help in completing
parts of this study. We thank Scott Steckbauer who helped in the field, and we thank
1007
Heidi Snell who helped in nearly all phases
of the project. This study was conducted
while the senior author was a John Simon
Guggenheim Foundation Fellow.
REFERENCES
Andrews, R. M. and O.J. Sexton. 1981. Water relations of the eggs of Anolis auratus and Anolis limifrons. Ecology 62:556-562.
Ar, A., C. V. Pagenelli, 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.
Burghardt, G. M. and A. S. Rand, (eds.) 1982. Iguanas of the world: Their behavior, ecology, and conservation. Noyes Publications, N.J.
Ewert, M. A. 1979. The embryo and its egg: Development and natural history. In M. Harless and
H. Morlock (eds.), Turtles: Perspectives and research,
pp. 333-413. John Wiley and Sons, Inc., New
York.
Ferguson, G. W. and C. H. Bohlen. 1978. Demographic analysis: A tool for the study of natural
selection of behavioral traits. In N. Greenberg
and P. D. MacLean (eds.), Behavior and neurology
of lizards, an interdisciplinary colloquium, pp. 227248. U.S. Department of Health, Education, and
Welfare, Washington, D.C.
Fox, S. F. 1978. Natural selection on morphological
phenotypes of the lizard Uta stansbunana. Ecology 59:834-847.
Hoyt, D. F. 1976. The effect of shape on the surfacevolume relationships of birds' eggs. Condor 78:
343-349.
Huey, R. B., E. R. Pianka, and T. W. Schoener. (eds.)
1983. Lizard ecology: Studies of a model organism.
Harvard University Press, Cambridge.
Movchan, N. A. and N. S. Gabaeva. 1967. On the
antibiotic properties of the egg envelopes of grass
frogs (Rana temporaria) and steppe turtles (Testudo horsfieldi). Herpetol. Rev. 1:6.
Packard, G. C. and M. J. Packard. 1980. Evolution
of the cleidoic egg among reptilian antecedents
of birds. Amer. Zool. 20:351-362.
Packard, G. C , M. J. Packard, and T. J. Boardman.
1981. Patterns and possible significance of water
exchange by flexible-shelled eggs of painted turtles (Chrysemys picta). Physiol. Zool. 54:165-178.
Packard, G. C, T. L. Taigen, T. J. Boardman, M. J.
Packard, and C. R. Tracy. 1979. Changes in
mass of softshell turtle (Tnonyx spinerus) eggs
incubated on substrates differing in water potential. Herpetologica 35:78-86.
Packard, G. C, C. R. Tracy, and J. J. Roth. 1977.
The physiological ecology of reptilian eggs and
embryos, and the evolution of viviparity within
the class Reptilia. Biol. Rev. 52:71-105.
Packard, M. J., G. C. Packard, and T. J. Boardman.
1980. Water balance of the eggs of a desert lizard
(Callisaurus draconoides). Can. J. Zool. 58:20512058.
1008
C. R. TRACY AND H. L. SNELL
Rahn, H. and A. Ar. 1974. The avian egg: Incuba- Tracy, C. R. 1976. A model of the dynamic exchanges
tion time and water loss. Condor 76:147-152.
of water and energy between a terrestrial
Romer, A. S. 1959. The vertebrate story. University of
amphibian and its environment. Ecol. Mongr. 46:
Chicago Press, Chicago.
293-326.
Shine, R. 1980. "Costs" of reproduction in reptiles. Tracy, C. R. 1980. On the water relations of parchOecologia 46:92-100.
ment-shelled lizard (Sceloporus undulatus) eggs.
Copeia 1980:478-482.
Snell, H. L., H. M. Snell, and C. R. Tracy. 1984.
Variation among populations of Galapagos land Tracy, C. R. 1982. Biophysical modelling in reptilian
iguanas (Conolophus): Contrasts of phylogeny and
physiology and ecology. In C. Gans and F. H.
ecology. Biol. J. Linn. Soc. 21:184-207.
Pough (eds.), Biology of the Reptilia, pp. 75-321.
Academic Press, London.
Snell, H. L. and C. R. Tracy. 1985. Behavioral and
morphological adaptations by Galapagos land Tracy, C. R., G. C. Packard, and M.J. Packard. 1978.
iguanas (Conolophus subcristatus) to water and
Water relations of chelonia eggs. Physiol. Zool.
energy requirements of eggs and neonates. Amer.
51:378-387.
Zool. 25:1009-1018.