Chemical Composition of Egg Shell

.
Biol. Rm . (1977). 52. p p 71-105
7'
BRCPAH 52-3
THE PHYSIOLOGICAL ECOLOGY OF REPTILIAN

EGGS AND EMBRYOS. AND THE EVOLUTION OF
VIVIPARITY WITHIN THE CLASS REPTILIA
BY GARY C PACKARD. C. RICHARD TRACY AND JAN J . ROTH

Department of Zoology and Entomology. Colorado State University.
Fort Collins. Colorado 80523. USA
(Received 27 July 1976)
CONTENTS
.
.
PAGE
I Introduction
I1 Morphology of reptilian eggs
. . . . .
. . . .
I11. Water relations of reptilian eggs .
(I) Uptake of water from soil .
. . . .
. . . .
(a) Parchment-shelledeggs .
(b) Calcareouseggs
. . . . . .
(2) Mechanism ofwater transport into eggs
. .
. .
(3) Adaptive significanceofwater uptake .
IV Sources of minerals for embryos .
. . . .
. . . .
V Patterns of nitrogen excretion .
VI . Exchangeofgases
. . . . . . .
. . .
(I) The atmosphere adjacent to eggs .
(2) Themechanismof gasexchange .
. . .
VII Temperature and metabolism .
. . . .
(I) Effects of temperature .
. . . . .
. . . . .
(2) Metabolism of embryos
VIII Egg retention and the evolution of viviparity
. .
(I) Distribution of the live-bearing method
. .
(2) A model for the evolution of viviparity .
. .
. . .
(3) Adaptive value of egg retention .
( a ) Temperature benefits
. . . . .
(b) Water for embryonic development
( c ) Food for emergent young
. . . .
. .
(d) Protection of developing embryos .
(e) Arboreal and aquatic habits of adults
. .
(4) Evolution of placentation
. . . . .
( 5 ) Why are there no viviparous turtles or crocodilians?
IXSummary .
. . . . . . . .
X Acknowledgements .
. . . . . .
XI References .
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I INTRODUCTION
Natural selection presumably operates on all stages in the life-cycle of an animal. and
so embryos. as well as adults. can be expected to exhibit adaptations to the environments in which they occur. Moreover. the success of a natural population often
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
72
Table
I.
HZgher levels of classifiation of surviving members of the

class Reptilia
Subclass Anapsida
Order Chelonia turtles, terrapins, and tortoises
Subclass Lepidosauria
Order Rhynchocephalia the tuatara, Sphenodm punctatus
Order Squamata - lizards, snakes, and amphisbaenians
Subclass Archosauria
Order Crocodilia - alligators, crocodiles, and gavials
depends as much upon adaptations of embryonic stages as upon adaptations of adults,

and thus a consideration of the problems of embryonic existence is an essential component of any full account of the ecology of an animal.
Our objective in preparing the present review of the physiological ecology of
reptilian eggs and embryos is to seek a greater understanding of the adaptations of
these embryos (and therefore of reptiles generally) to their physical environments.
Unfortunately, the literature on this subject is relatively sparse, many published
accounts on the biology of reptilian embryos are anecdotal, and reported studies
frequently have suffered from the use of inappropriate experimental designs and/or
inadequate analytical procedures. Nevertheless, we shall draw some conclusions from
the available data, and shall also identify several testable hypotheses for future
research.
11. MORPHOLOGY OF REPTILIAN EGGS
Oviparity presumably represents the ancestral mode of reproduction in the Class

Reptilia (Table I), for even the embryos of viviparous snakes and lizards possess an
egg-tooth, thereby reflecting their derivation from oviparous ancestors (Bellairs, I970).
Oviparous reproduction characterizes the tuatara, all living Crocodilia and Chelonia,
and most species of the Squamata (Bellairs, 1959,1970). Nevertheless, a substantial
number of lizards, snakes, and amphisbaenians have assumed a live-bearing habit
(Bellairs, 1959),and numerous other species of the Squamata exhibit modes of reproduction that may represent intermediate stages in the evolutionary transition from
oviparity to viviparity.
The amniotic eggs of reptiles have long been regarded as similar to those of birds
(Bellairs, I970). Unfortunately, this generalization may have obscured important
biological differences between the eggs of Crocodilia and Chelonia on the one hand,
and those of Lepidosauria on the other. These differences pertain to the eggshell, the
egg (or shell) membranes, and the albumen layer.
Eggs of Crocodilia are virtually identical to those of birds (Fig. I). The calcareous
eggshell is thick and hard (Voeltzkow, 1892;Reese, 1915; Bigalke, 1931; Guggisberg,
1972;Singletary & Ogden, 1973),and is comprised of crystals of calcite (Erben, 1970;
Jenkins, 1975)between which there exists a matrix of proteinaceous fibres (Erben,
1970;Jenkins, 1975). The crocodilian eggshell is penetrated by numerous pores
(Reese, 1915;Bigalke, 1931; Erben, 1970)that apparently allow respiratory gases to
Physiological ecology of reptilian embryos
73
AVES
membrane
CHELONIA AND
CROCODlLlA
Blastodisc
Vitelline
mem brane
membrane
LEPIDOSAURIA
Blastodisc
Shell
Albumen
Vitelline
membrane
Fig. I. Schematic diagrams illustrating the major morphologic features of the eggs of Aves
(upper), Crocodilia and Chelonia (middle), and Lepidosauria (lower). Although a space is shown
here between the tertiary membranes of avian, crocodilian, and chelonian eggs for clarity of
illustration, the egg membranes of avian eggs are actually adherent except in the region of the
air space, and homologous membranes in crocodilian and chelonian eggs are adherent throughout. See teXt for references.
diffuse between the enclosed embryo and the nest environment (see Section VI, 2). A
pair of tertiary egg membranes separates the eggshell from a thick layer of albumen
(Clarke, 1891; Voeltzkow, 1892; Reese, 1915; Bigalke, 1931; Erben, 1970; Jenkins,
1975). Bigalke (193I) reported that an air space forms between the outer egg membrane
and the eggshell during developmentof embryonic crocodiles (Crocodylus niloticzrs),but
Reese (1915) and McIlhenny (1935) contended that there is no air space in eggs of
alligators (Alligator mississippiensis) at any time during development. Since eggs of
crocodilians seem to absorb water and to swell during the course of natural incubation
(McIlhenny, 1934, 1935; Guggisberg, 1972), thereby precluding formation of an air
space (Romijn & ROOS,1938), we suspect that the eggs examined by Bigalke (1931)
74
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
were not developing normally at the time of study, and therefore predict that an air
space does not usually form in eggs of crocodilians.
The eggshell is also well developed in eggs of Chelonia (Fig. I), but varies from
being hard and brittle, as in tortoises and some fresh-water turtles (e.g. Lynn & von
Brand, 1945; Young, 1950), to being soft and pliable (parchment-like) as in other
species (e.g. Cunningham, 1922; Tomita, 1929; Lynn & von Brand, 1945; Legler,
1960; Bustard, 1972). The calcium salts of the eggshell are in the form of aragonite
crystals (Young, 1950; Erben, 1970), between which there is a matrix of proteinaceous
fibres (Simkiss & Tyler, 1959; Erben, 1970). The outer surface of the shell of tortoise
(Testudo graeca) and soft-shelled turtle (Trionyx euphraticus) eggs seems to be covered
with a thin cuticle similar to that which occurs on the eggs of many birds (Young,
1950; Simkiss & Tyler, 1959), but a cuticle probably does not occur on eggshells of
most Chelonia (Giersberg, 1922; Simkiss & Tyler, 1959). Both calcareous and parchment-like eggshells are penetrated by a large number of pores that presumably provide
for a diffusive exchange of respiratory gases (Young, 1950; Erben, 1970). Two tertiary egg membranes lie between the thick layer of albumen and the eggshell (Young,
1950; Simkiss, 1962;Erben, 1970; Ackerman & Prange, 1972). An air space has been
observed in the hard, calcareous eggs of the tortoise, Testudograeca (Young, 1950),but
the eggs of most Chelonia seem to absorb water and to swell during normal incubation (see p. 75), thereby precluding formation of an air space (Romijn & ROOS,1938).
Thus, an air space probably is not of general occurrence in the eggs of Chelonia.
Eggs of oviparous LepidosauriaFig. I ) (usually have a flexible, parchment-like shell
containing relatively small amounts of calcium carbonate (Dendy, 18993; Bellairs,
I 959, 1970). However, gekkonid lizards of the subfamilies Gekkoninae and Sphaerodactylinae characteristically produce eggs with relatively hard, calcareous shells
(Bustard, 1968a), as do lizards of the family Dibamidae (Boulenger, 1912).
The parchment-like shell of lepidosaurian eggs seems to be formed from a single
shell membrane comprised of approximately five layers of minute fibres (Giersberg,
1922; Jacobi, 1936; Tracy, Roth & Packard, unpublished), with crystals of calcium
carbonate deposited between fibres in outer layers of this membrane (Giersberg, 1922 ;
Harris, 1964). Pores, such as exist in the shells of chelonian and crocodilian eggs, seem
not to occur in eggshells of Lepidosauria (Tracy, Roth & Packard, unpublished).
No other membranes seem to be present on the inner aspect of the shell of lepidosaurianeggs(Dendy, 1899b; Giersberg, 1922;Weekes, 1935;Fisk &Tribe, 1949). The
albumen layer in eggs of these reptiles is exceedingly small at the time of oviposition
(Dendy, 1899b; Giersberg, 1922; Jacobi, 1936; Clark, 1946; Fisk & Tribe, 1949;
Harris, 1964; Badham, 1971), but seems to increase in volume during the course of
normal incubation owing to the absorption and storage of water (see Section 111, I ) .
There is no air space in parchment-shelled eggs of Lepidosauria at any time in
development (Dendy, 1899b; Harris, 1964).
Calcium carbonate is not deposited in the shell of eggs produced by live-bearing
lizards and snakes (Weekes, 1935; Bellairs, 1959; Hoffman, 1968), but the shell
membrane usually persists - albeit in varying degrees of evolutionary reduction
(Giersberg, 1922; Jacobi, 1936). Presence of the shell membrane frequently has been

75
used as the criterion to distinguish ovoviviparity from true viviparity (Hoffman,
1968, 1970), but other criteria (e.g. mass of yolk present in the egg, or role of maternal
secretions in nourishing developing young) have occasionally been used to characterize
these modes of reproduction (Bellairs, 1959, 1970; Salthe & Mecham, 1974). However, intermediate stages can be found between ovoviviparity and true viviparity
by any of the commonly applied sets of criteria, and so any attempt to distinguish
between these patterns of reproduction inevitably tends to obscure details that are
important in considerations of the evolution of the live-bearing habit. Therefore, we
prefer to use the term viviparous to describe any reptile giving birth to free-living
young.
Many viviparous lizards and snakes exhibit rather complex forms of placentation
(Weekes, 1935; Bauchot, 1965; Hoffman, 1968), but in most of these species the large
mass of yolk provided by the female parent at ovulation is the primary (or only) source
of nourishment for the developing embryo (Weekes, 1935). No species of viviparous
reptile is known to produce alecithal eggs such as occur in mammals.
111. WATER RELATIONS OF REPTILIAN EGGS
(I) Uptake of water from soil

(a) Parchment-shelled eggs
Brimley (1903) and Dendy ( 1 8 9 9 ~were
)
among the first to observe that parchmentshelled eggs of Lepidosauria and Chelonia swell during the course of incubation, and
observations confirming this phenomenon have been made repeatedly since their early
work (e.g. Giersberg, 1922; Lynn & von Brand, 1945; Shaw, 1952). The swelling is
attributable to absorption of water by eggs from the substrate upon which they rest
(Giersberg, 1922; Cunningham & Hurwitz, 1936; Cunningham, Woodward &
Pridgen, 1939; Lynn & von Brand, 1945; Clark, 1946, 1 9 5 3 ~ Mulherkar,
;
1962;
E r s t , 1971).With few exceptions, however, these studies have been performed in the
laboratory on substrates of unknown water potential (see p. 78), and so there is some
question as to whether or not the conditions of experimentation simulated conditions
found in natural nests. For this reason, it seems that generalizations concerning water
absorption by parchment-shelled reptilian eggs may be somewhat premature (e.g.
Bellairs, 1959, 1970).
Few observations seem to have been made of parchment-shelled eggs incubating in
natural nests. Eggs of the sea turtle, Chelonia mydas, apparently absorb water and swell
during the first 24 h after oviposition (Bustard, 1972), but it is not clear whether the
eggs continue to imbibe water during the remainder of incubation, particularly since
most of the eggs are not in actual contact with the moist sand forming the walls of the
nest cavity (Hendrickson, 1958). Also, Whitaker (1968) indicated that eggsof the lizard,
Leiolopisma suteri, increase in volume during their natural incubation, so that the eggs
become firmly wedged inside the incubation chamber ;presumably, such swellingsterns
from absorption of water.
Eggs of oviparous reptiles seldom are deposited in situations where soil comes into
contact with all surfaces of the eggs; and even in those species using a subterranean
76
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
chamber for oviposition, the volume of the nest cavity greatly exceeds that of the
contained eggs (Allard, 1935;McIlhenny, 1935 ;Cagle, 1950; Brown, 1956; Hendrickson, 1958; Muth, 1976). Since viable eggs lose water continuously, even when
;
incubated in an atmosphere saturated with water vapour (Clark, 1946, 1 9 5 3 ~ Fitch
& Fitch, 1967)~
water must evaporate constantly from the surfaces of eggs into the nest
atmosphere. It may seem anomalous that water can be lost from reptilian eggs to a
saturated atmosphere, but the probable explanation of this phenomenon is relatively
simple (Adolph, 1932). Metabolic heat produced by the embryo developing within an
egg raises the temperature of the egg and eggshell slightly above that of the surrounding mass of air in the nest cavity. Thus, the vapour pressure of water in the eggshell is
greater than that of the surrounding air, and this difference in vapour pressure drives
the evaporation of water from the egg surface to the atmosphere (see Monteith, 1973:
chapter 9).
Eggs taken from natural nests seldom show signs of desiccation (i.e. shrunken or
flaccid appearance, dented or wrinkled surface). Nevertheless, the eggs must have
been losing water continuously to the nest atmosphere, and so the only possible explanation for their generally turgid state is that they were absorbing water from the substrate (Clark, 1946, 1953u). In so far as the rate of water absorption exceeded the rate
of water loss by evaporation, the eggs swelled; but even eggs exhibiting no change in
weight and/or volume during development must have absorbed significant quantities
of water from the substrate to compensate for evaporative water loss from the exposed
surfaces. This line of reasoning, while admittedly indirect, constitutes the strongest
evidence that parchment-shelled eggs absorb water during the course of natural
incubation.
I n some laboratory studies, parchment-shelled eggs have been reported to increase
in size at rates which remain constant throughout development (e.g. Reynolds, 1959;
Pandha & Thapliyal, 1967; Ernst, 1971; Dixon, Staton & Hendricks, 1975), whereas
in other instances the rates of change in size have been claimed to increase (Cunningham & Huene, 1938;Harris, 1964; Garg, Pandha & Thapliyal, 1967) or to decrease
(Blanchard, 1927; Lynn & von Brand, 1945;Mulherkar, 1962; Dmiel, 1967; Badham,
1971; Subba Rao & Rajabai, 1972) during the course of incubation. Additionally, eggs
of several species of Chelonia and Squamata have been observed to exhibit a sudden
decline in weight and/or dimensions in the days immediately prior to hatching (Blanchard, 1927; Cunningham & Hurwitz, 1936; Cunningham & Huene, 1938; Reynolds,
1959; Gordon, 1960; Bustard & Greenham, 1968; Whitaker, 1968; Dixon et al., 1975),
whereas eggs of other species have been observed to swell appreciably just before
hatching (Harris, 1964). Unfortunately, it is difficult to attach much significance to
these several observations, for information has not been reported on the water potential of substrates in natural nests or of those upon which eggs were incubated in the
laboratory. Thus, we cannot conclude that conditions of laboratory study simulated
conditions occurring in nature.
77
(b) Calcareous eggs

Even the hard, calcareous eggs produced by certain reptiles may exhibit a net
uptake of water during normal incubation (McIlhenny, 1935 ; Guggisberg, 1972).The
most convincing evidence on this point was gathered by McIlhenny (1934), who
periodically opened a natural nest of the alligator, Alligator mississ@piensis,to examine
eggs developing therein. McIlhenny noted cracks in eggs when he opened the nest 6
weeks after oviposition, and the cracks had enlarged and widened when the nest was
again visited z weeks later. Thus, the eggs under observation apparently were swelling
during incubation, presumably owing to a net uptake of water from the moist walls of
the nest chamber. Calcareous eggs experiencing a net increase in water content probably would not have an air space (Romijn & ROOS,
1938),and so the reports that no air
space forms in alligator eggs can be regarded as further evidence that a net uptake
of water normally occurs in eggs of Crocodilia (Reese, 1915;McIlhenny, 1935).
Bustard( 1971b) recorded an increasein weight of crocodile (Crocodylusnovaeguineae)
eggs incubated on a moist substrate, but seemingly normal young also hatched from
two eggs that experienced a net water loss during the course of development.
Unfortunately, it is difficult to draw conclusions from these observations, because we
cannot determine which of the sets of incubation conditions most closely approached
those to which eggs are exposed in natural nests; and the number of eggs used was
extraordinarily small in any case.
Evidence concerning the uptake of water by the calcareous eggs of certain Chelonia
is equivocal. Eggs of a soft-shelled turtle (Trionyx triunguis) experienced a 10% increase in weight when incubated on a moist substrate (Mendelssohn, cited by Dmiel,
1967),but calcareous eggs of the turtle, Kinosternm subrubrum, seemed not to absorb
water when incubated under superficially similar conditions (Lynn & von Brand,
1945). Information on water potentials of egg contents and of substrates was not
presented in either of the preceding investigations, and so we are unable to draw conclusions from these studies concerning the water metabolism of turtle embryos
developing within calcareous eggs. The observation by Young (1950)of an air space
in eggs of the tortoise, Testudo graeca, indicates that the eggs experienced a net loss
of water after oviposition (Romijn & ROOS,1938), but the eggs probably were not
developing normally at the time they were examined (Young, 1950).
Calcareous eggs of gekkoninine and sphaerodactylininegeckos are especiallyinteresting with regard to their water relations, for these eggs have been described as being
cleidoic (Bustard, 1968b). Since a cleidoic egg experiences a mass exchange only of
gases with its environment, there is, by definition, no absorption of water from the
substrate. Therefore, water lost from the surfaces of such an egg cannot be replaced,
and must be drawn from water reserves present in the egg at the time of oviposition.
We would be interested to learn whether the calcareous eggs of geckos have a large
* The term cleidoic, which is not equivalent to amniotic, seems to have been used first by
Needham, in 1931, in describing the avian egg: The avian egg is thus, in the strictest sense of the
word, a closed box, with walls which can only be penetrated by matter in the gaseous state. The term
cleidoic is suggested for this state of affairs... (Needham, 1963: p. 1615).
...
78
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
volume of albumen, in contrast to eggs of other squamate reptiles, or whether water

reserves are sequestered in other compartments of the eggs.
Mechanism of water transport into eggs

Movement of water from the substrate into an egg must occur by diffusion of
liquid water through the eggshell from a region of high water potential (the substrate) to a region of low water potential (the contents of the egg). Two factors determine the water potential of an egg: (i) the pressure potential of the contained liquids,
and (ii) the osmotic potential of these same liquids (Salisbury & Ross, 1969; see also
Rose, 1966). For our purposes, pressure potential can be regarded as being equivalent
to turgor pressure of the egg, and will generally have a positive value. Osmotic potential, on the other hand, is the component of water potential that becomes increasingly
negative as embryonic liquids become more concentrated with solute. For an egg to
absorb water, the potential of water in the substrate must exceed the algebraic sum
of the pressure potential and the osmotic potential of the egg contents.
The rate of water movement into an egg is directly related to (i) the difference between the water potential of the substrate and that of the egg contents, (ii) the surface
area and hydraulic conductance of the egg, and (iii) the hydraulic conductivity of the
material comprising the substrate upon which the egg rests (Tracy, 1976). These
several factors affecting water transport into reptilian eggs can be expressed formally by
the following equation:
me =
(Yf3Oll - Y e g g )
(2)
where me = water uptake by the egg (g.min-l), (Ysoil

-Yegg)
= the difference in water
potentials of the egg and the substrate upon which it rests (bars), A, = the surface
area of the egg in contact with the substrate (cm2),K, = the hydraulic conductance of
the egg (g.cm-2. min-l .bar-l), and ksoil = the hydraulic conductivity of the substrate
(g.cmW2.
min-l .bar-l .cm-l). The term A s e represents the total hydraulic conductance of the egg, whereas the companion term ( ~ ? T A , ) ~ represents
~~A~,,~
the
~ total
hydraulic conductance of the soil (Tracy, 1976).
Examination of this equation reveals several interesting properties of water transport
into reptilian eggs. If an egg has the ability to take up water faster than the soil can
supply it, the egg can cause the soil to become drier with time, and the rate of water
uptake by the egg will decline owing to the reduced ability of dry soils to conduct
water to the egg surface (Gardner, 1965). On the other hand, if both the egg and the
soil conduct water at high rates, the egg will tend to take up water until its water
potential approximates that of the soil. Thus, the complex array of determinants of
water transport into reptilian eggs provides many ways for different species to adapt to
different environmental conditions (e.g. by selecting nest sites in different types of
soil or in soils with different water tables, by changing the conductance or geometry
of the eggshell, etc.). Therefore, we believe that a biophysical approach to the study of
water relations of reptilian eggs promises to yield important biological insights that
were not forthcoming from earlier work.
79
Conversely, consideration of the physical determinants of water transport reveals the

difficulty of designing and interpreting experiments concerned with the water relations of reptilian eggs. Clearly, a number of factors influencing water transport may
vary simultaneously, thereby complicating studies of water dynamics. Furthermore,
eggs of most reptiles apparently lose water by evaporation while simultaneously
absorbing liquid water from the substrate (p. 76), and so the ratio of egg surface
exposed to the atmosphere relative to the surface in contact with the substrate may
substantially influence the equilibrium weight of the egg or its viability in different
experimental settings. These problems make it very difficult to interpret the findings
of the many laboratory studies that have been reported in the literature.
Developing reptilian embryos apparently influence the uptake of water from the
substrate (Giersberg, 1922). For instance, eggs of the lizard, Agama ugama, that have
been killed by exposure to strong sunlight fail to swell when placed in contact with
liquid water, whereas viable eggs swell in the expected manner (Harris, 1964).
Additionally, parchment-shelled eggs containing dead embryos frequently can be
identified by a loss of turgidity (Mayhew, 1963; Ortleb, 1964; Bustard & Greenham,
1968). Although Legler (1960) reported that infertile eggs of the turtle, Tewapene
urnata, may swell for as much as 2 weeks before beginning to shrivel, it is possible
that the eggs he observed contained embryos which died after completing only 14
days of development.
There is some evidence that water absorption by eggs is related to the temperature
at which they are incubated. Eggs of hognose snakes (Heterodon platyrhinos and
Heterodon nasicus) incubated at 26.7 "C absorb water much more rapidly than eggs
held at 23-3 "C (Platt, 1969), and similar observations have been made on eggs of the
snake, Carphophis vermis, incubated at different temperatures (Clark, D. R., 1970).
Although the rate of swelling may therefore be related to the rate of embryonic metabolism (Section VII, I), these findings do not provide indisputable support for the
idea that embryos influence the uptake of water from the environment. For instance,
an increase in temperature would cause hydraulic conductivity of the substrate also
to increase (Gardner, 1968), and this factor alone could cause water uptake to proceed
more rapidly.
Fluctuations in the hydric environment to which eggs are exposed may also have an
important influence upon the overall uptake of water during incubation. Eggs of the
colubrid snakes, Elaphe guttata and Spalerosophis cliSJordi, absorb more water when
exposed alternately to moist and to dry substrates than when they are held continuously on a moist substrate (Clark, I953a; Dmi'el, 1967)' again raising the possibility
that embryos exercise some form of control over the uptake of water from the environment. However, a complete biophysical analysis of water fluxes is required before
other, purely physical, explanations of this phenomenon can safely be ruled out.
Much of the water absorbed by eggs of lizards and snakes is incorporated into the
albumen fraction (Clark, 1953b; Badham, 1971). The volume of the albumen increases progressively during incubation (Fig. 2), and at the time of hatching the
albumen may comprise nearly 15 per cent of the mass of the entire egg (Clark, D. R.,
1970). For water to diffuse through the eggshell and into the albumen, the water
G. C . PACKARD,
C. R. TRACY
AND J. J. ROTH
80
0 0
0
0
0
10
20
30
40
50
60
70
Age (days)
Fig. 2. Volume of albumen in eggs of the oviparous snake, Colder constrictor, at different times
after oviposition. Data are from Clark (19536).
100
9-
-?
8-
7-
6-
&J
00
0
10
20
30
40
50
60
70
Age (days)
Fig. 3. Cumulative plots of nitrogen excreted as ammonia (A), urea (0)

and uric acid (+) by
embryos of the oviparous snake, Colder constrictor, at different stages of development. Data are
from Clark (1953b).
potential of the albumen must be lower than that of water in the substrate. Packard
(1966) suggested that the urea, which is the primary nitrogenous waste produced by
embryos of the oviparous snake, Coluber constrictor, and which is sequestered mainly
in the albumen fraction of eggs (Clark, 1953b), may play an important role in water
absorption. Since metabolism of developing embryos is a continuous source of urea in
this species (Fig. 3), the water potential of the albumen could be held relatively low
throughout incubation (Clark, 1953b), and a continuous uptake of water might therefore result (Fig. 2). However, Badham (1971) recently presented evidence that unhydrated proteins are added to the albumen of developing eggs of the lizard, Amphibolurus burbatus, thereby indicating that important interspecific differences may exist
81
in the means by which embryos of the Squamata influence the water potential of their
egg contents.
As a parchment-shelled egg swells during incubation, it becomes more and more
turgid (Dendy, 1899a; Cunningham & Huene, 1938; Reynolds, 1959; Clark, D. R.,
I 970), suggesting that pressure potential of the embryonic liquids increases throughout development (Giersberg, 1922); and such an increase in hydrostatic pressure
would tend to oppose movement of water into the egg. Simultaneously, however, the
surface area of the eggshell would increase, and the thinning of the eggshell (Jacobi,
1936; Platt, 1969) could lead to slight increases in the conductance of the egg to
water. While these factors doubtless have an influence on water transport into incubating eggs, the major determinants of water movement are likely to be the osmotic
potentials of soil water and egg contents, and the hydraulic conductance of the substrate (Tracy, 1976).
(3) Adaptive szjpificance of water uptake

In most instances, failure of an egg to swell during incubation should not be taken
to indicate that the egg was not absorbing water, as some workers have supposed
(Dmiel, 1967), but only that an equilibrium was reached between water uptake and
water loss. On the other hand, swelling of an egg indicates that water was absorbed in
excess of that required to replace water lost by evaporation.
There is considerable disagreement concerning the possible adaptive significance
of water absoption and storage by reptile eggs. Some investigators believe that water
accumulated within an incubating egg constitutes little more than a buffer against
the dangers of potential desiccation (Fitch & Fitch, 1967; Badham, 1971; Bustard,
1971a, b), and that uptake and storage of water is not essential for normal development
of the embryo (Bustard, 1966; Dmiel, 1967). Conversely, other workers contend that
absorption and storage of water is of utmost importance to the developing embryo
(Gordon, 1960).
We believe the weight of the evidence supports the contention that water absorption
is a critical factor in the normal development of reptilian eggs. Hatchlings of the
lizard, Anolis carolinensis,were found to be larger and heavier when hatched from eggs
incubated continuously on moist substrates than when they emerged from eggs subjected to mildly desiccating conditions (Gordon, 1960). Such data do not demonstrate
that water absorbed from the environment is incorporated into embryonic protoplasm,
but they do indicate that water absorption has survival value.
In some investigations, hatchlings have been reported to weigh less than freshly
laid eggs (Lynn 82: von Brand, 1945; Mendelssohn, 1963, 1965; Bustard, 1967;
Dmiel, 1967; Clark, D. R., 1970; Badham, 1971),leading several authors tacitly to
conclude that water absorbed by eggs is not incorporated into forming tissue. Before
arriving at such a conclusion, however, it is essential to consider the mass of the eggshell and other extra-embryonic materials that are discarded at hatching, and to
take into account the oxidation of organic material in embryonic metabolism (Cunningham et al., 1939; Lynn & von Brand, 1945). Furthermore, other studies have
shown that hatchlings of many species of lizards, snakes and turtles weigh more than
6
B R E 52
82
G. C . PACKAFW,
C. R. TRACY
AND J. J. ROTH
freshly laid eggs (Cunningham & Huene, 1938; Brown, 1956; Mendelssohn, 1963;
Bustard, 1965)~
which is possible only in the event that a portion of the water absorbed
by the eggs was incorporated into the protoplasm of the embryos.
A. V. Fitch (1964) discovered living embryos of the lizard, Eumeces obsoletus, in eggs
that had shrivelled from desiccation, prompting a later suggestion (Fitch & Fitch,
1967) that uptake of water by eggs is of minor importance to the developing young.
However, evidence presented by A. V. Fitch (1964) indicates only that there was a net
loss of water from incubating eggs, and not that water uptake was not occurring.
Additionally, the nature of her study precluded incubating eggs from hatching, and so
it remains to be shown that embryos of Eumeces obsoletus can withstand desiccation
without ill effect. Indeed, it is important to note that turtle eggs subjected to desiccation early in incubation experience extraordinarily high mortality, whereas eggs
subjected to dehydration later in development - while not experiencing high mortality
- frequently produce abnormal hatchlings (Lynn & Ullrich, 1950).
In summary, we tentatively conclude that water absorbed by eggs of reptiles is incorporated, in part, into the protoplasm of developing embryos, and that failure to
absorb water leads to smaller hatchlings and, possibly, to a higher incidence of developmental anomalies and embryonic death. In the case of Lepidosauria, the increase in
volume of the albumen accompanying water absorption may have further adaptive
value in preventing the invasion of the eggs by bacteria (Board & Fuller, 1974).
IV. SOURCES OF MINERALS FOR EMBRYOS
Earlier studies of the eggs and hatchlings of the sea turtles, DermocheZys cmiacea and
Lepidochelys olivacea, revealed that hatchlings contain 3-5 times more calcium than is
present in the yolk and albumen of eggs at the time of oviposition (Simkiss, 1962,
1967). These observations led several investigators to examine the possibility that a
portion of the calcium required for ossification of bones of embryonic reptiles is taken
up from the substrate incidental to water absorption. Evidence now available indicates
that all of the calcium (and magnesium) required by developing embryos is present in
eggs at the time of oviposition (Cunningham et al., 1939; Bustard & Greenham, 1968;
Jenkins & Simkiss, 1968; Bustard, Simkiss & Jenkins, 1969; Jenkins, I975), but two
fundamentally different means for providing this element seem to exist.
Embryos of crocodilians and chelonians, like those of birds, recover large quantities
of calcium from the inner surface of the eggshell during the course of development
and in this way largely satisfy their requirements for this element in ossification of
bones (Bustard et al., 1969; Jenkins, 1975). The yolk is a rich source of magnesium
for embryonic chelonians (Bustard et al., 1969)~but the source of magnesium for
embryonic crocodilians has yet to be determined.
In contrast, embryos of snakes and lizards, including those geckos producing
calcareous eggs, appear to obtain both calcium and magnesium from rich stores
present in the yolk (Jenkins & Simkiss, 1968), and recover little (if any) mineral from
the eggshell. Use of the yolk, rather than the eggshell, as the reservoir for calcium
may have been a critical factor allowing viviparity to evolve in many species of the
Squamata (see Section VIII, 5).
83
+
O0.4
' I
A
O+
At
10
20
30
40
Age (days)
50
60
70

embryos of the oviparous lizard, Calotes versicolor, at different stages of development. Values
are estimated from data presented by Athavale & Mulherkar (1967).
V. PATTERNS OF NITROGEN EXCRETION
The various patterns of nitrogen excretion among adult vertebrates generally are
thought to represent adaptive strategies related to the availability of water in the
environment (Campbell, 1973). Ammonia, which is the usual end product of protein
metabolism in aquatic animals, is detoxified by incorporation into urea or uric acid in
amphibious and terrestrial species. Urea is highly soluble and can be retained internally for variable periods of time with no apparent ill effects, but substantial
quantities of water are required intermittently as a vehicle for eliminating the stored
waste. Conversely, uric acid (or urates) is relatively insoluble and can be eliminated
with a minimal loss of water.
Unfortunately, few studies have dealt with the patterns of nitrogen excretion of
reptilian embryos, even though available data suggest the existence of a spectrum of
adaptive responses among embryos of different species. Additionally, contrary to the
oft-cited prediction of Needham (1963: 1132 ff.), the patterns of nitrogen excretion
exhibited by reptilian embryos seem frequently to differ from those characterizing
adults.
Embryos of the oviparous snake, Coluber constrictor, are ammoniotelic for the first
10 days of development (Fig. 3), producing and releasing relatively large quantities of
ammonia gas, but then begin to channel the bulk of their amino nitrogen into urea
(Clark, 1g53b). Uric acid is not produced in significant amounts until just before
hatching, at which time the embryos seem to experience a biochemical metamorphosis
'in anticipation' of the new suite of physiological demands attending a free-living
existence (Packard, I 966). Data reported for the oviparous snakes, Psammophis
6-2
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
84
9r
8h
A
A
7-
5 6-
A
0
-0
J 5-
4-
A 0
% 3-
!F
2
o +
AA
2-
? 4,
+
1-
0 :
4-
.I.
10
20
30
40
50
60
Age (days)

embryos of the American alligator (Alligator Pn;ssippiensis) at different stages of development.
Data are from Clark et al. (1957).
schokari and Psammophis sibilans, are an inadequate basis for generalization concerning the patterns of embryonic nitrogen excretion in these species (Haggag, 1964),but do
not differ conspicuously from those summarized in Fig. 3 for Coluber constrictor.
Embryos of the oviparous lizard, Calotes versicolor, may exhibit a pattern of nitrogen
excretion different from that described for embryonic snakes (Athavale & Mulherkar,
1967). Ammonia seems not to be an important excretory product in embryos of this
species (Fig. 4; the high values for ammonia at 25 and 35 days of age are most likely
due to experimental error), and urea and uric acid account for about equal amounts of
the nitrogen excreted at all stages of development. We should mention, however,
that it is not clear from the report by Athavale & Mulherkar (1967) whether the entire
content of eggs was used in their analyses. In particular, the albumen fraction, which
is a major repository for urea in eggs of other reptiles (Clark, 1953 b), may not have
been sampled in this study of Calotes eggs, and certain of the nitrogenous materials
may therefore have been underestimated.
Careful examination of the extra-embryonic membranes in eggs of the oviparous
lizard, Agama agama, failed to reveal any sign of crystals of uric acid (or urate),
indicating that embryos of this species probably produce large quantities of ammonia
and/or urea during development (Harris, 1964).
Embryos of the sea turtle, Lepidochelys olivacea, produce significant amounts of
urea throughout development (Tomita, 1929), and the small quantities of uric acid
that accumulate in eggs of this species probably originate in purine catabolism. Although ammonia production was not measured by Tomita, the continuous decline in
nitrogen content of incubating eggs (Nakamura, 1929) indicates that ammonia (in the
form of a gas) may be the primary excretory product throughout embryonic development of this species.

0
0
0
0
0
.$ 0.3
o.l
0
0 0
0
A
A
0.2
A
~
tI
++++
+++
?+
10
20
30
40
50
60
70
80
Age (days)
embryosof theviviparoussnake, Thammphistirtulis, at differentstagesof development.Data are
from Clark & Sisken (1956).
The pattern of nitrogen excretion manifest by embryos of the alligator, Alligator

mksz+piensis, is of special interest, since development proceeds inside hard, calcareous eggs. Contrary to expectation (Needham, 1963)) little uric acid is produced by
embryos of this species (Fig. 5 ) ) and it seems likely that the urate originates in purine
catabolism rather than in deamination reactions. Amino nitrogen seems to be divided
evenly between ammonia (in the form of ammonium ions) and urea for the entire
course of embryonic development (Clark, Sisken & Shannon, 1957).
Embryos of the viviparous snake, Thamnophis sirtalk, exhibit a pattern of nitrogen
excretion quite similar to that described earlier for embryos of oviparous snakes
(Clark & Sisken, 1956). Small amounts of ammonia (in the form of ammonium ions)
and uric acid accumulate in the tissues and extra-embryonic membranes of developing embryos, but the embryos clearly are ureotelic throughout the period of development (Fig. 6). Although the production of urea and ammonia by embryos may have
been underestimated somewhat in consequence of transplacental movement of these
solutes (Clark & Sisken, 1956; see also Clark, Florio & Hurowitz, 1955; Hoffman,
1970)) we doubt that the placental exchange of these materials is so extensive as to
alter our conception of the pattern of embryonic nitrogen excretion in this species.
In summary, uricotelism is not common among reptilian embryos, even in species
developing within calcareous eggs. Ammonia may be an important excretory product
in embryos of some species, especially in early stages of development, but all species
studied so far rely heavily upon urea as an end product in protein catabolism. Since
urea is an osmotically active material, use of this compound as an end product in
86
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
protein catabolism has important implications concerning the water metabolism of

reptilian embryos.
VI. EXCHANGE OF GASES
(I) The atmosphere adjacent to eggs

The eggs of oviparous reptiles usually are deposited in sheltered sites beneath rocks
and other objects, or are buried in sand, friable soil, or decaying vegetation. Unfortunately, information is as yet unavailable on the atmosphere to which eggs of most
reptiles are exposed; but with the possible exception of eggs incubating in soils with
much humus where microbial respiration may reduce the oxygen content of the air in
interstitial spaces, we suspect that the composition of air adjacent to eggs usually does
not depart appreciably from that of the overlying atmosphere, even when the eggs are
deposited in subterranean nests (see Seymour, 1973).
A known exception to our prediction concerns those reptiles depositing large numbers of eggs in a single nest chamber that may be at a considerable depth below the
surface of the ground. For example, there seems to be a pronounced depletion of oxygen, and an accumulation of carbon dioxide, in the atmosphere inside nests of sea
turtles (Ackerman & Prange, 1972; Prange & Ackerman, 1974). Apparently, oxygen is
consumed by the large mass of eggs more rapidly than it can be replenished by diffusion through the interstitial spaces in the substrate (Prange & Ackerman, 1974). The
influence, if any, of such hypoxic and hypercarbic conditions on embryonic development remains to be determined.
(2) The mechanism of gas exchange

The exchange of gases between a reptilian embryo and its environment presumably
is by diffusion. In Crocodilia and Chelonia, oxygen apparently diffuses inward
through pores in the eggshell (Reese, 1915; Bigalke, 1931; Young, 1950; Erben,
1970), and then through spaces between fibres of the two egg membranes (Fig. I). In
Lepidosauria, however, molecules of gas seem simply to diffuse through spaces
between fibres of the shell membrane (Fig. I).
Using methods developed in studies of gas exchange across shells of avian eggs,
Ackerman & Prange (1972) estimated the permeability of the shell and outer egg membrane of sea turtle (Chelonia mydm) eggs to oxygen. The mean value for the
permeability of their preparations was 6-59 x I 0-6 cm3.sec-l .cm-2. torr-I, a value
approximately twice that reported for similar preparations from eggs of the domestic
fowl (Wangensteen, Wilson & Rahn, 1970/71). Since the thickness of the shell (which
is taken as an approximation to the length of the diffusion pathway) does not differ
appreciably between eggs of sea turtles and those of the domestic fowl (Wangensteen
et al., 1970/71;Ackerman & Prange, 1972), the shell of turtle eggs seems to have a
total pore area approximately twice that of chicken eggs.
Regrettably, the preceding value for the permeability of sea-turtle eggs to oxygen
may be of limited use in constructing models of the process of gas exchange. Ackerman & Prange (1972) failed to consider the possibility that in turtle eggs, as in bird
eggs, the inner egg membrane constitutes a major barrier to the diffusion of oxygen
87
(Kutchai & Steen, 1971), and so their data probably cannot be used to estimate the
total barrier to diffusive uptake of oxygen by eggs from the surrounding atmosphere.
Rand (1968) studied rates of water loss from eggs of the domestic fowl and crocodiles
(Crocodylw acutus), and noted that the rate of water loss (expressed as a percentage of
the original egg weight) was only slightly greater in crocodile eggs than in chicken eggs.
Assuming that the eggs of these two species were of about the same size, the data
indicate that the permeability of the shell of crocodile eggs to water vapour (and
presumably to other gases) is almost indistinguishable from that of chicken eggs.
Unfortunately, the characteristics of oxygen transport into eggs of crocodilians
cannot be predicted from data on permeability of these eggs to water vapour because
the inner egg membrane probably constitutes an important barrier to diffusion of oxygen, but not to water vapour (Kutchai & Steen, 1971). I n chicken eggs, the permeability of this membrane to oxygen increases during the course of incubation, owing
to the withdrawal of water from spaces between the fibres of the membrane (Kutchai
& Steen, 1971). However, since eggs of crocodilians absorb and store water during
the course of normal development (Mcllhenny, 1934, 1935 ; Guggisberg, 1972),
there may be no change in water content of the inner membrane between oviposition
and hatching, and so resistance to inward diffusion of oxygen may not change during
incubation of crocodilian eggs. The possibility that the permeability of egg membranes
to oxygen does not increase during incubation of crocodilian eggs raises important
questions pertaining to metabolism and acid/base balance of developing embryos (see
Erasmus, Howell & Rahn, 1970/71), and therefore merits further study.
Since the eggs of lepidosaurians seemingly have no pores in the eggshell through
which respiratory gases can diffuse, gas exchange must occur by diffusion between the
fibres of the shell membrane. We predict that surfaces of eggs exposed to the nest
atmosphere are involved in gas exchange, with oxygen moving inwards through airfilled spaces between the fibres of the shell membrane, but that surfaces in contact
with (or in proximity to) the substrate - and which are involved in water transport into
the eggs - are of little importance in gas exchange because the interstices of the shell
membrane are filled with liquid water. A corollary of this hypothesis is that some fraction of the egg surface must not be in contact with the moist substrate, for uptake of
oxygen would be inhibited if diffusion had to occur through water-filled spaces in the
shell membrane. Such a circumstance would lead to a reduction in the rate of metabolism and development of the embryo, and could conceivably result in suffocation.
These contentions receive some support from a study of eggs of the lizard, Amphibolurus barbatus, in which eggs that were completely covered with moist sand (and
therefore were wetted on all surfaces) took longer to complete incubation than eggs
incubated on the surface of the sand (Bustard, 1966). Further support for our contentions comes from observations that parchment-shelled eggs of turtles suffer
extraordinarily high mortality when soil or sand comes into contact with all surfaces of
the eggs (Cagle, 1950; Simon, 1975).
88
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
VII. TEMPERATURE AND METABOLISM
(I) Effects of temperature

Embryonic reptiles seem to behave like 'typical' ectothermic organisms in their
physiological responses to temperature. Metabolism increases with temperature
(Zarrow & Pomerat, 1937), and development of embryos to hatching proceeds much
more rapidly in warm environments than in cool surroundings (Legler, 1960 ;Yntema,
1960; Dmi'el, 1967; Goode & Russell, 1968; Platt, 1969; Clark, D. R., 1970; Vinegar,
1973; Sexton & Marion, 1974). For example, an increase in incubation temperature of
I "C shortens the incubation period for embryonic hognose snakes (Heterodon
nasicus) by 7 days (or 1 0 % ; Platt, 1969), and a rise of temperature from 27.8 "C to
32.8 "C leads to the completion of embryonic development of box turtles (Terrapene
ornata) in 59 days instead of 70 days (Legler, 1960).
Although development may proceed over a range of temperatures, there appears
to be a particular temperature for each species at which embryogenesis proceeds
optimally. Relatively small deviations in temperature from the optimum frequently
lead to an increase in the incidence of developmental anomalies, but the anomalies
usually are so minor (e.g. changes in number of scale rows) as to escape notice (Fox,
1948; Fox, Gordon & Fox, 1961; Osgood, 1968; Bustard, 1969b; Moll & Legler,
1971; Vinegar, 1973, 1974). However, relatively large departures of the incubation
temperature from the optimum usually result in the formation of chimeric embryos
(Yntema, 1960; Osgood, 1968; Vinegar, 1974), and embryonic mortality generally
increases appreciably (Licht & Moberly, 1965; Bustard, 1971a, b; Vinegar, 1973;
Sexton & Marion, 1974). Embryos of tropical species are less tolerant of departures
from their thermal optimum than are embryos of temperate forms (Licht & Moberly,
1965; Vinegar, 1973).
Despite the fact that developmental abnormalities and embryonic death result from
prolonged exposure of eggs of temperate reptiles to temperatures falling several
degrees below the optimum, further reductions in temperature generally lead to arrested
development, which can be tolerated with no apparent ill effect other than a slight
delay in the time of hatching (Cunningham, 1922; Fitch, 1954; Legler, 1960; Yntema,
1960; Maderson & Bellairs, 1962). Indeed, the Australian tortoise, Chelodina expansa,
deposits eggs in the autumn, and the eggs lie dormant in the soil throughout the
winter months, during which time soil temperatures decline to 5 "C (Goode & Russell,
1968) and embryogenesis presumably is fully arrested (Cunningham, 1922; Yntema,
I 960). When temperatures increase in the following spring, development of the tortoise embryos begins (or resumes), and normal young subsequently hatch from the
eggs. If temperatures in the soil during the winter were not low enough to arrest
embryogenesis completely, developmental anomalies would be expected to occur
(Yntema, 1960).
The duration of exposure of eggs to temperatures departing from the optimum
seems to be important, but this subject has not been fully explored. Brief exposure
of lizard and snake eggs to high and low temperatures indicates that embryos of temperate forms can withstand extremes similar to those withstood by adults of the same
89
species (Fitch, 1964; Fitch & Fitch, 1967), but the range of tolerable temperatures
seems to diminish as the length of exposure increases (Fitch & Fitch, 1967). The
ability briefly to withstand high and low temperatures is clearly of adaptive value, in
that excursions in nest temperature during midday and at night will not alter the
course of development significantly.
However, most reptilian embryos are probably not exposed to wide fluctuations in
temperature, either during the course of a single day or during the entire course of
embryogenesis, owing to the moderating effects of the nest in which the eggs usually
are laid (Reese, 1915; Brown, 1956; Goode & Russell, 1968; Bustard, 1969a; Rand,
1972; Chabreck, 1973; Van Devender & Howard, 1973). Temperatures in nests of the
American alligator (Alligator mississtppiensis) vary during the course of a single day
through a range of only 1.2 "C, whereas die1 variation in air temperature above the
nests may be as much as 9-3 "C (Chabreck, 1973). Also, nests of the tropical lizard,
Iguana zjpana, are reported to have temperatures of 3 1-32 "C for extended periods, and
to exhibit virtually no daily variation (Rand, I 972) ; these observations are consistent
with data indicating a limited tolerance of embryos of this species to fluctuations in
temperature (Licht & Moberly, 1965).
Sea turtles may present an important exception to the preceding generality. Die1
variation in temperature of nests of the turtle, Chelonia mydas, is less than z "C
(Hendrickson, 1958; Carr & Hirth, 1961;Bustard & Greenham, 1968;Bustard, 197z),
but the mean temperature in nests increases steadily from about zg "C at the time of
oviposition to nearly 35 "Cjust before hatching (Hendrickson, 1958). Also, a gradient
in temperature of as much as 2 "C usually is established between the centre of a mass of
eggs and the periphery of the nest (Bustard, 1972). The increase in mean temperature
of the nest, and the formation of a temperature gradient betweenthe inside and the outside of the nest, presumably stems from metabolic heat production of the large number
of embryos concentrated in the nest chamber (Hendrickson, 1958; Bustard, 1972).
Since eggs in the centre of a sea-turtle nest must undergo incubation at slightly
higher temperatures than are experienced by eggs at the periphery, it is reasonable to
assume that development of centrally located eggs is completed before that of other
eggs in the nest (Bustard, 1972). However, young in centrally located eggs apparently
delay hatching (or emergence) until litter mates located on the periphery of the nest
have completed development. The high degree of synchrony in the emergence of
young from a given nest results from a form of social facilitation in which the hatching
and digging movements of each individual are 'reinforced' by the activity of adjacent
animals (Carr & Hirth, 1961; Bustard, 1972).
Metabolism of embryos
At temperatures approaching the optimum for development, oxygen consumption
of turtle embryos increases with age in general conformity with the sigmoid growth
curve (Lynn & von Brand, 1945), and metabolism of advanced embryos is virtually
identical to that of hatchlings (Lynn & von Brand 1945; Prange & Ackerman, 1974).
Metabolism of snake embryos also increases with age, but the observed pattern of increase is exponential rather than sigmoid (Clark, I953C; Dmi'el, 1970); the failure of
(2)
G. C . PACKARD,
C. R. TRACY
AND J. J. ROTH
90
Table
2.
Summary of the modes of reproduction characterizing families of

the order Squamata
(From Fitch, 1970,with additional information from Boulenger, 1912, and Broadley, 1974)Only those
families are listed for which reliable information is available. For convenience, the classification scheme
used here is the same as was used by Fitch (1970).
All species
oviparous
Family
Amphisbaenidae
Gekkonidae
Iguanidae
Agamidae
Chamaeleontidae
Xantusiidae
Teiidae
Lacertidae
Scincidae
Dibamidae
Cordylidae
Gerrhosauridae
Anguidae
Anniellidae
Xenosauridae
Helodermatidae
Varanidae
Typhlopidae
Leptoty phlopidae
Uropeltidae
Acrochordidae
Boidae
Colubridae
Elapidae
Hydrophiidae
Viperidae
Crotalidae
Both modes of
reproduction
present
All species
viviparous
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
investigators to detect an inflection point in plots of oxygen consumption against age

may simply indicate that metabolism of snake embryos does not begin to stabilize until
just before hatching (Dmiel, 1970).
In a study of five species of colubrid and viperid snakes, the average slope of double
logarithmic plots of oxygen consumption versus mass of the embryos was 0.65 (Dmiel
I 970), but the biological significance of this value is not clear. Interestingly, embryos of
many snakes seem to exhibit circadian cycles in metabolism, with peak metabolism
occurring during the day-time in embryos of diurnal species and at night-time in
embryos of nocturnal forms (Dmiel, 1969).
VIII. EGG RETENTION AND T H E EVOLUTION OF VIVIPARITY
Distribution of the live-bearing method

Fitch (1970)has recently compiled and analysed data on the incidence of viviparity
among living reptiles, and his monograph serves as an excellent source of information
on this subject.
(I)
91
Data summarized in Table z indicate that viviparity has arisen independently in

several different families of the reptilian order Squamata, and so the mode of reproduction characterizing different species of lizards, snakes and amphisbaenians has little
value as an index to their phylogenetic affinities. For instance, oviparity and viviparity
characterize different congeneric species of such lizards as Eumeces (Scincidae),
Gmrhonotus (Anguidae), and Sceloporus (Iguanidae), and of such snakes as Agkistrodon
(Crotalidae), Natrix (Colubridae), and Vipera (Viperidae).
Of special interest are those species in which some populations may be characterized
by oviparity and others by viviparity, for insight may be gained from these species
concerning the adaptive value of the evolutionary transition to the viviparous state.
For example, the skink, Mabuya quinquetaeniata,is believed to be viviparous in South
Africa, but oviparous elsewhere in its range (Fitch, 1970). Likewise, the Central
American iguanid, Scelopmus variabilis, which is oviparous in most areas where it is
found (Fitch, 1970), may be viviparous at higher elevations in the Mexican state of
Veracruz (Werler, 1951);and the vipers, Echis carinata and Aspis vipera, are reported
to be oviparous in some localities and viviparous in others (Mendelssohn, 1963, 1965).
Unfortunately, variation between populations of squamate reptiles in their mode of
reproduction is not a well-documented phenomenon, and many of the accounts in the
literature are suspect. For instance, the most frequently cited example is the lizard
Lacerta vivipara, which is widely believed to be oviparous at lower elevations in the
Pyrenean Mountains in the south of France, and to be viviparous elsewhere in its range
(Fitch, 1970). In early September of 1924, Lantz (1927) discovered approximately 60
parchment-shelled eggs beneath a large stone situated in relatively moist terrain.
When the eggs were handled, young lizards emerged from several, and these hatchlings were immediately recognized as Lacerta vivipara. The other eggs in the nest
contained embryos at various stages of development, including some that had completed only about half of their embryogenesis. Since more than 12 females must have
been involved in laying so many eggs, Lantz (1927) suggested that oviparity may
characterize certain populations of the species.
Lantzs observations have never been confirmed, despite the fact that nearly 50
years have passed since publication of his report (Bellairs, 1970). Since Lantz did not
actually observe any instance of oviposition, and since he did not state that the unhatched eggs from the nest contained living embryos, it is possible that he drew
incorrect conclusions from his observations. I n unfavourably cool years - of which
1924 may have been one, judging from the late date on which the communal nest was
discovered (see Blanchard & Blanchard, 1940) - young female Lacerta vieripma may
prematurely expel some of their developing young while retaining the remainder of
their eggs until the completion of embryogenesis (Panigel, 1956; see also Hoover,
1936). Eggs expelled prematurely have a parchment-like appearance owing to the fact
that they do not have the usual layer of mucus on the surface of the shell membrane,
and they probably do not survive long because of rapid desiccation (Panigel, 1956).
Thus, it is possible that some of the parchment-shelled eggs discovered by Lantz
were moribund eggs deposited prematurely by females responding in an unusual
way to the generally inclement weather conditions, and that the remaining eggs-
92
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
containing full-term young - were coincidentally deposited beneath the same rock
by other lizards of the same species shortly before Lantzs arrival.
(2) A
model for the evolution of viviparity

Doubtless there is variation within natural populations of most reptiles both in the
thickness of eggshells and in the normal interval during which eggs reside in the oviducts of the female before deposition. When both relatively thin eggshells and relatively long retention of eggs in utero characterize the reproductive effort of certain
females, there is the potential for evolution of viviparity, the only requisites being
that the thickness of eggshells and the period of intra-uterine retention are heritable
characteristics, and that females exhibiting these traits contribute disproportionately
to succeeding generations.
The simplest model for the evolution of viviparity from oviparity therefore entails a
gradual increase (over many generations) in the length of time eggs are retained in the
oviducts of the females prior to deposition, during which time development of the
embryos proceeds at near-optimal rates. Thus, the evolutionary transition from oviparity to viviparity leads to eggs being laid at progressively more advanced stages of
development, and consequently, the interval from oviposition to hatching is progressively reduced. The final stage in this sequence occurs when females deposit eggs containing fully formed young which then emerge from within the enclosing shell and
extra-embryonic membranes.
A survey of the reproductive biology of contemporary reptiles yields information
that is consistent with the preceding evolutionary model. For instance, eggs of many
reptiles pass through the oviducts rather slowly (see Reese, 1915;Hamlett, 1952;
Cooper, 1965; Clark, D. R., 1970).During transit, embryonic development usually
proceeds - limited only by the requirements of the embryos for favourable temperatures, an adequate exchange of respiratory gases, a means for excreting nitrogenous wastes, and a source of water. Consequently, at the time of oviposition, eggs of
many reptiles contain embryos in various stages of organogenesis. A known exception
to this generality pertains to Crocodilia and Chelonia, whose embryos seem not to
proceed past gastrulation before oviposition, regardless of how long the eggs are
retained in the oviducts (Cunningham, 1922;McIlhenny, 1934,1935; Risley, 1944;
Lynn & von Brand, 1945;Legler, 1960;Decker, 1967);and we shall return to this
point shortly.
In certain species of the Squamata, eggs spend so much time in the oviducts of
females that the species appear to be in evolutionary transition from oviparity to viviparity. Eggs of the lizard, Lacerta muralis, are carried by females for about one month
after fertilization occurs (Cooper, 1965),and approximately 42% of the incubation
period of worm snakes, Carphqhis vermis, is spent in the oviducts of the female parent
(Clark, D. R., 1970).Embryos of the garden lizard, CaZotes versicolor, have advanced
to a stage of development comparable to a 55-60 h chick embryo by the time the eggs
are laid (Muthukkaruppan, Kanakambika, Manickavel & Veeraraghavan, I 970). Eggs
of the Australian skink, Saiphos equalis, are reported to hatch within a few days of
93
laying (Fitch, 1970), a feat that is matched by the 4-day incubation period of some
eggs produced in northerly populations of the snake, Opheodrys vernalis (Blanchard,
1933).
The lizard, h e r t a wiwipara, retains eggs internally for the full period of development. The eggs can be removed surgically from females and successfully incubated
in vitro on gauze moistened with saline (Panigel, 1956; Holder & Bellairs, 1962;
Maderson & Bellairs, 1962). The young hatching from such eggs appear normal in
every respect (Panigel, 1956), and thus females of this species seem to do little more
than provide a favourable thermal, hydric, and gaseous environment in which their
eggs can develop.
One striking morphological change during the transition from oviparity to viviparity
among squamate reptiles appears to be a reduction in the degree of calcification of the
eggshell and in the thickness of the shell membrane. In a population of green snakes,
Opheodrys vernalis, characterized by retention of eggs within the oviducts of females
for most of the period of incubation, the eggshells are described as being unusually
thin and delicate (Blanchard, 1933). Also, eggs of the oviparous lizard, Lacerta ugiZis,
have a lightly calcified eggshell, whereas those of the viviparous congener, Lacerta
vivipma, are completely uncalcified (Jacobi, 1936); and the shell membrane is much
thicker in eggs of the former species than in eggs of the latter (Jacobi, 1936). Indeed,
while the shell membrane persists in eggs of most viviparous lizards, snakes and amphisbaenians, in no instance is the membrane known to be impregnated with calcium
salts (Weekes, 1935; Bellairs, 1959).
While eggs are retained in the oviducts of the female parent, the embryos benefit
from the moderate thermal environment provided by the mother (see p. 94), and
excretion of nitrogenous wastes probably presents no major problem since urea can
either be stored in embryonic and/or extra-embryonic fluids or be allowed to diffuse
out of the eggs into the oviducts. Also, water can be absorbed by eggs from the fluid
environment (Giersberg, 1922; Jacobi, 1936; Tinkle, 1973; Newlin, 1976), passing
directly into the yolk (Badham, 1971)rather than into an albumen fraction.
The major problem of intra-uterine existence is probably the exchange of gases,
and this problem may underlie the reduction in calcification and thickness of the eggshell attending the evolutionary transition from oviparity to viviparity. Since respiratory gases apparently diffuse through the liquid environment of the oviducts,
through the calcareous layer of the eggshell, and between the fibres of the egg or shell
membranes, the diffusion pathway may be relatively long, and the metabolism of the
developing embryos could be inhibited by a low rate of uptake of oxygen by the eggs.
Consequently, a reduction in the extent of the diffusion barrier imposed by the eggshell and associated membrane(s) may be essential if the metabolism of the embryos is
to be sustained, particularly in later stages of development when oxygen requirements
are liely to be high (Lynn & von Brand, 1945; Clark, 1 9 5 3 ~Dmiel,
;
1970; Prange
& Ackerman, 1974).
Support for the contention that adaptive thinning of the eggshell and associated
membrane(s) is necessary if intra-uterine development of reptilian embryos is to be
sustained comes from studies of the metabolism of developing snakes. Embryos of the
94
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
oviparous snake, Elaphe guttata, either accumulate an oxygen debt during later stages
of intra-uterine existence, or the rate of embryonic metabolism (and growth) is
depressed, owing to inadequate uptake of oxygen from the immediate environment
(Clark, 1952, 1953a); either of these alternatives suggests that intra-uterine development of embryos would not proceed much further without some reduction of the
diffusion barrier imposed by the eggshell and shell membrane. Furthermore, it is
important to note here that embryonic development of Crocodilia and Chelonia is
arrested while eggs are retained within the oviducts of the female, possibly because
uptake of oxygen from the immediate environment is insufficient to sustain embryogenesis (Risley, 1944; Lynn & von Brand, 1945); and thick shells characterize eggs of
both the Chelonia and the Crocodilia.
(3) Adaptive value of egg retention

(a) Temperature benejits
We conceive of egg retention as conferring special advantage to relatively Kselected* reptiles (eggs cannot be retained for long intervals by animals producingmore
than one clutch per year) dwelling in thermally seasonal environments, particularly at
high latitudes and altitudes. Assuming that the enzymes of developing embryos have
the same thermal optima as the enzymes of the female parent, the adult animal can,
by regulating her body temperature behaviourally at an optimal level for physiological
functions, incidentally provide an optimal thermal environment for the offspring
developing within her body. Thus, during the warmth of the day, she may move
into warm parts of the environment and maintain a relatively high and constant body
temperature, whereas at night she may retreat to sheltered sites where neither she
nor her eggs will be exposed to particularly low temperatures. Were this female to
deposit her eggs in a nest where daytime temperatures rose sufficiently high to support
embryogenesis at high rates, the eggs presumably would be exposed to nocturnal temperatures sufficiently low to induce anomalous development (Vinegar, 1973, 1974).
Conversely, were she to deposit the eggs in a more protected site (the usual circumstance), where they would not be exposed to potentially harmful nocturnal
temperatures, diurnal temperatures in the nest presumably would be suboptimal for
development, and hatching would be delayed accordingly.
Retention of eggs internally for brief periods would enable embryos to attain a given
stage of development more rapidly than embryos of conspecific females that do not
retain eggs for the same length of time. Thus, if all embryos have similar rates of
development following oviposition, those eggs subjected to longer intervals of retention inside the female parent would hatch earlier than other eggs of the species. Early
hatching may have adaptive significance in allowing young more time to feed and to
grow before entering hibernacula for the first time (see Cagle, IIJ~O),
or early hatching
may assure that young are not trapped (and killed) in the nest by early winter storms
(Risley, 1933). Thus, genetic variation among females in the length of time for which
* The term K-selected, which comes from the logistic model for population growth, refers to
populations of organisms characterized by relatively long Iife-spans, delayed maturity, and iteroparity
(Tinkle, 1969; Pianka, 1970).
95
eggs are held in the oviducts could provide the basis for an evolutionary transition to
viviparity stemming from thermal benefits to the embryos.
Evidence in support of the preceding evolutionary hypothesis is largely circumstantial, but persuasive nonetheless. As indicated earlier, relatively high and constant
temperatures, closely approaching the optimum for a species, provide for rapid
embryonic development (Blanchard & Blanchard, 1940; Legler, 1960; Yntema, 1960;
Dmi'el, 1967; Goode & Russell, 1968; Platt, 1969; Clark, D. R., 1970; Vinegar, 1973;
Sexton & Marion, 1974) that is relatively free of thermally induced anomalies (Fox,
1948; Yntema, 1960; Fox et al., 1961; Osgood, 1968; Vinegar, 1973, 1974). It is
therefore important to note that pregnant female garter snakes (Thumnophis sirtalis,
a viviparous species) have somewhat higher body temperatures in nature than either
males or non-gravid females (Stewart, 1965). Moreover, gravid female water snakes
(Nutrix fmciata and Natrix taxispilota, which also are viviparous) seem to maintain
body temperatures within a narrower range than other individuals of these species
(Osgood, I 970). Furthermore, when spiny lizards (Sceloporuscyanogenys, which again
are viviparous) are placed in a thermal gradient in the laboratory, pregnant females
cease basking at slightly lower body temperatures than do other animals; and these
females change position in the thermal gradient less often than other lizards, suggesting that their body temperatures fluctuate relatively little during the course of a day
(Garrick, 1974). These several observations on viviparous reptiles are indicative of the
kinds of benefits that might accrue to embryos of oviparous species at intermediate
stages in the evolutionary transition to viviparity.
The green snake (Opheodrys vernalis) provides a possible example of the evolutionary transition to viviparity in response to low temperatures and/or a relatively short
growing season. In northern Michigan (ca. 45-5"N latitude), the thin-shelled eggs of
this species are laid in advanced stages of development, and hatching occurs about 2
weeks after oviposition (and in some instances in as little as 4 days; Blanchard, 1933).
In contrast, in a more southerly region (ca. 42O N latitude), eggs of this species require
about 3 0 days between deposition and hatching (Stille, 1954). Apparently, cooler conditions and/or a shorter growing season in northern Michigan have led to the evolution
of longer periods of egg retention by females in that population because of the thermal
benefits accruing to the developing embryos (Packard, 1966).
I n some species of oviparous lizards producing two clutches of eggs a year, eggs of
the second clutch are retained longer in the oviducts of the female than eggs of the
first clutch (Shaw, 1952; Sexton & Marion, 1974). Consequently, at the time of oviposition, eggs of the second clutch contain embryos in more advanced stages of development than were present in eggs of the first clutch at the time of oviposition; and the
interval from conception to hatching presumably is reduced for embryos of the second
clutch. Eggs of the first clutch have ample time for development to proceed to completion, even if they are deposited in nests where temperatures are slightly below the
optimum for embryogenesis. However, eggs of the second clutch must complete
development within a shorter span of time, and must hatch before the advent of unfavourable weather in the autumn of the year (Sexton & Marion, 1974). Thus, retention of eggs of the second clutch may be adaptive in providing for accelerated growth
96
G. C . PACKARD,
C. R. TRACY
AND J. J. ROTH
of those embryos in the relatively favourable thermal environment afforded by the

maternal oviducts, thereby assuring completion of embryogenesis in what effectively
constitutes a short growing season.
In the past, patterns of geographic distribution of oviparous and viviparous Squamata have been cited as evidence that viviparity often has arisen in response to temperature stresses on embryos (Weekes, 1933, 1935 ; Duellman, 1965; Packard, 1966;
Greer, I 968 ; Greene, I 970). The predominance of viviparous species in reptilian
faunas found at high altitudes and latitudes, and the converse at low altitudes and
latitudes, is compelling evidence that the live-bearing mode of reproduction confers a
major adaptive advantage on species occupying cool environments. However, it is
quite possible that the live-bearing habit evolved elsewhere, in response to different
selection pressures, and that viviparity simply preadapted many reptiles for occupancy of cool climates (Tinkle, I 967). Distributional patterns of contemporary
lizards, snakes and amphisbaenians may therefore be of little value in identifying the
selective agent responsible for driving the evolutionary transition from oviparity to
viviparity.
(b) Waterfor embryonic development

Many lizards (Anderson, I 962; Gehlbach, 1965), turtles (Cagle, 1950; Legler, 1960)
and crocodilians (Reese, 1915)retain eggs in their oviducts until favourable conditions
exist for oviposition. The critical factor in the environment seems to be soil moisture,
for egg-laying frequently follows a rainfall.
This correlation between the advent of rain and oviposition has led some authors to
suggest that, in some species, the evolutionary transition from oviparity to viviparity
may have been driven by inadequate supplies of water in the substrate for the support
of embryogenesis (Goin & Goin, 1971). The implication of this hypothesis is that
rainfalls do not recharge dry substrates with sufficient water to sustain eggs to hatching. Thus, according to this evohtionary model, reIatively eaily conception, coupled
with a period of intra-uterine development of the embryos, results in the deposition
of eggs, following a rainfall, that contain young in relatively advanced stages of development; and these young can successfully complete embryogenesis and hatch during
the relatively short interval when there is adequate moisture in the soil to satisfy their
physiological requirements.
We find no direct evidence, however, that soils recharged with water by rain dry
rapidly enough to become limiting to the successful development of reptilian eggs, and
so the aforementioned hypothesis describing the evolution of viviparity in response to
insufficient soil moisture remains unsupported. Nevertheless, retention of eggs until
the advent of rain clearly has adaptive value, for eggs deposited in dry soils may
succumb, even if they are exposed only briefly to desiccating conditions. Thus, a
slight delay in the time of oviposition could assure that eggs are deposited under the
most favourable conditions possible for embryonic development (Anderson, 1962).
However, retention of eggs until the advent of rain would not necessarily lead to the
acquisition of viviparity. If rain provides adequate substrate moisture for the complete
development of eggs, then there exists no selective force to produce the progressive
97
reduction in shell thickness that is required if intra-uterine development is to proceed

and if the interval from oviposition to hatching is to be reduced. I n other words, there
is no apparent advantagein substituting the moist environment of the maternal oviducts
for the moist environment of the soil when soil moisture is sufficient to sustain
embryogenesis. On the other hand, if it can be shown that there are environments in
which the substrate dries so rapidly after a rainfall that extended periods of extrauterine development are precluded, then a relatively short period of extra-uterine
incubation would be a necessary preadaptation for the existence of a reptilian population in that area. But in either case, it seems unlikely that factors relating to soil water
could provide the necessary selective forces to effect a progressive shortening of extrauterine incubation leading to viviparity (Section 111, 2).
Our explanation for the adaptive significance of retaining eggs until the advent of
rain has the advantage of applying not only to squamate reptiles, where there exists an
evolutionary potential for adoption of viviparity, but also to chelonians and crocodilians, in which intra-uterine development of embryos seems not to be possible
(Cunningham, 1922;McIlhenny, 1934,1935;Risley, 1944;Lynn & von Brand,
1945;Legler, 1960;Decker, 1967).
(c) Food for emergent young

In regions characterized by seasonal rainfall, where the onset of the rainy season is
a predictable event (i.e. it is closely correlated with Zeitgebers such as photoperiod and
temperature), viviparity may have arisen in some species as an adaptation providing
for more effective use of a seasonal food resource by the emergent young. Insectivorous lizards are the most likely candidates for responding to selection pressures of
this type.
Shortly after the advent of a rainy season a myriad of insects usually emerge
(Janzen, 1973),and the seasonal appearance of this abundant food resource could be
the basis for selection to drive a transition from oviparity to viviparity among
reptiles capable of responding to these pressures. Those individuals in a population
that mate relatively early, and whose embryos develop within the body of the female
parent, will deposit eggs at the beginning of the rainy season capable of completing
embryogenesis sooner than eggs of conspecifics that mate relatively late. Early emergence would afford the young an opportuNty to exploit the abundant food resource
more fully than would be possible for late-hatching individuals. Consequently, earlyhatching young may reach a larger size by the return of seasonally inclement conditions, or they may attain reproductive maturity sooner than late-hatching animals.
Either of these factors could be of survival and subsequent reproductive value.
( d ) Protection of developing embryos

Retention of eggs by the female can be regarded as a form of maternal behaviour
that is an effective alternative to brooding eggs in a nest. Whenever the probability of
mortality to eggs in the nest is greater than the probability of death to eggs in the
maternal oviducts, there could be selection for prolonged periods of egg retention
(Neill, 1964;Fitch, 1970).The ability of the female either to evade potential predators
7
B R E 52
98
G. C . PACKARD,
C. R. TRACY
AND J. J. ROTH
or to defend herself against such enemies increases the likelihood that intra-uterine
eggs also will survive. Thus, assuming that embryogenesis could proceed while eggs
are retained within the oviducts, selection again could act upon variation in the normal
time of oviposition to effect an evolutionary transition from oviparity to viviparity.
(e) Arboreal and aquatic habits of adults

Some workers have contended that specialization of certain species for either
arboreal or aquatic modes of existence has led to the adoption of viviparity, for it
clearly is adaptive for such animals not to have to leave their native element in order to
reproduce successfully (Neill, 1964; Fitch, 1970). However, it seems more reasonable
to conclude that prior acquisition of the live-bearing mode of reproduction was an
important preadaptation that allowed these animals to specialize for arboreal or aquatic
existence (see Tinkle, 1967). For example, arboreal and aquatic reptiles would be freed
from the requirement to construct nests and lay eggs only when viviparity had been
achieved; and there is no apparent selection pressure (other than those already discussed) that could lead to progressively longer periods of egg retention and intrauterine development of embryos in animals already specialized for arboreal or
aquatic existence.
( 4 ) Evolution of placentation
We shall not attempt an extensive discussion of the morphology and physiology of
reptilian placentae, for excellent accounts have appeared elsewhere (Weekes, 1935 ;
Bauchot, 1965; Hoffman, 1968). Briefly, both a yolk-sac placenta and a chorioallantoic
placenta are formed in most species of viviparous lizards, snakes and amphisbaenians ;
the yolk-sac placenta seems to be the primary site for uptake of water for the embryo,
whereas the chorioallantoic placenta plays the major role in gas exchange. In species
such as the viviparous lizard, Lacerta viut$ara, the placentae are poorly developed,
and the developing embryos absorb only water and oxygen by way of the respective
placental attachments (Panigel, 1956). In other species, small quantities of ions
(Conaway & Fleming, 1960; Hoffman, 1970) and amino acids (Clark et al., 1955;
Clark & Sisken, 1956) may pass from the mother to the developing young via the
placentae, and some metabolic wastes may pass in the opposite direction (Clark &
Sisken, 1956); but even in these forms the large mass of yolk is the main source of
energy and nutrients to support embryogenesis. In only a few species do the developing embryos appear to obtain a major quantity of nutrient material from the parent
via the placentae, and in these forms the mass of the yolk usually is reduced accordingly
(Weekes, I 93 5).
We regard the development of placentation as a natural extension of the adaptive
reductions in calcification and thickness of eggshells that occur in the evolution of
viviparity, and as adaptive initially in facilitating the transfer of water and respiratory
gases between the developing embryo and its environment. However, the acquisition
of placental attachments creates an opportunity for an evolutionary change in the role
of the female parent in providing nutrients for her developing young. Whereas in
oviparous species (and in most viviparous forms so far studied) there is a major energy
drain upon the female attending vitellogenesis, it is possible for females of species
99
exhibiting placentation to extend that same energy commitment over a longer interval
of time. Since the severe energy drain attending vitellogenesis of oviparous reptiles
may affect subsequent survival of the female, her prospects for survival and later reproduction may be increased considerably if she is able to avoid a drastic depletion of her
metabolic reserves immediately before ovulation.
( 5 ) Why are there no viviparous turtles or crocodilians?

Assuming that certain species of Chelonia and Crocodilia might have benefited
from the acquisition of viviparity, for any one of the several reasons detailed
previously, it is interesting to inquire Why arent there any viviparous turtles or
crocodilians?
Turtles and crocodilians probably lack the evolutionary potential to become viviparous because of an inability to effect adaptive reductions in the thickness of the eggshell to the degree required for the exchange of respiratory gases in the intra-uterine
environment. We tentatively suggest that the inability of these reptiles to experience
reductions in the thickness of the eggshell may have to do with the source of calcium
ions for the developing embryos. As indicated earlier (p. 82), embryonic Chelonia
and Crocodilia apparently mobilize mineral from the inner surface of the eggshell to
provide calcium for ossification of their skeletal elements (Bustard et al., 1969;
Jenkins, 1975)~and any major reduction in the calcium content of the eggshell presumably would adversely affect mineralization of forming bones. Thus, an adaptive
reduction in the degree of calcification of the eggshell, which is a necessary element in
the evolutionary transition from oviparity to viviparity, may be precluded in these
animals by the absence of an alternative source of calcium ions for the developing
embryos. I n other words, a major physiological adaptation of chelonian and crocodilian embryos for securing calcium ions from a ready and accessible reserve in the
eggshell may have specialized these organisms to the extent that they no longer have
the evolutionary potential to become viviparous.
In contrast, lizards, snakes and amphisbaenians are not so prevented from effecting
adaptive reductions in the mineral content of the eggshell, because the source of
calcium ions for developing embryos of the Squamata apparently is the yolk (Jenkins
& Sirnkiss, 1968); and it is among the Squamata where viviparity has evolved on
numerous occasions.
IX. SUMMARY
I . Eggs of Crocodilia and Chelonia, like those of birds, have a pair of egg membranes
separating a thick layer of albumen from the calcareous shell. In contrast, eggs of
oviparous Lepidosauria have only a single shell membrane, upon which relatively small
amounts of calcium carbonate are deposited; and the volume of albumen in eggs is
extraordinarily small at the time of oviposition.
2. With the possible exception of certain geckos and some chelonians, eggs of oviparous reptiles seem always to absorb water from the substrate during the course of
normal incubation. In so far as the rate of water absorption exceeds the rate of water
7-2
I00
G. C. PACKARD,
C. R. TRACY
AND J. J. ROTH
loss by transpiration from exposed surfaces, the eggs swell during incubation. The
term cleidoic cannot be used to describe eggs of this type.
3. Embryos of lizards and snakes influence the water potential of extra-embryonic
fluids contained within their eggs, thereby maintaining or increasing the gradient in
water potential that drives water absorption.
4. Embryos of Crocodilia and Chelonia obtain a substantial portion of the calcium
used in ossification of skeletal elements from the inner surfaces of the eggshell.
In contrast, embryonic lizards and snakes draw upon extensive reserves of calcium
present in the yolk, and obtain little (if any) calcium from the eggshell.
5 . All reptilian embryos seem to produce substantial quantities of urea as a detoxification product of protein catabolism. Contrary to expectation, uricotelism may not
be common among reptilian embryos, even in those few instances where development
takes place within a hard, calcareous egg.
6. In eggs of Crocodilia and Chelonia, respiratory gases seem to pass by diffusion
through pores in the calcareous eggshell and through spaces between the fibres of the
pair of egg membranes. No pores have been observed in the shell of lepidosaurian
eggs, and so gases presumably diffuse between the fibres of the single (multilayered)
shell membrane.
7. Metabolism of reptilian embryos is temperature-dependent, as is true for most
ectothermic organisms. For each species, there appears to be a particular temperature at which embryonic development proceeds optimally, and departures from this
optimum elicit increases in developmental anomalies and/or embryonic mortality.
8. Viviparity has evolved on numerous occasions among species of the Squamata,
but seemingly never among Crocodilia or Chelonia. Since the evolution of viviparity
entails a progressive reduction in the eggshell, only those organisms whose embryos
do not depend upon the eggshell as a source of calcium may have the evolutionary
potential to become viviparous.
9. Evolutionary transitions from oviparity to viviparity could have been driven by
selection related to (i) thermal benefits to embryos consequent upon retention of eggs
within the body of a parent capable of behavioural thermoregulation; (ii) protection of
the eggs from nest predators and/or soil microbes; and (iii) more effective exploitation of a seasonal food resource by early emerging young.
X. ACKNOWLEDGEMENTS
Several of our colleaguesand students have rendered invaluable assistance to us in the preparation of
this review. In particular, we want to acknowledge our debt to Henry S. Fitch, Richard E. Jones, William C. Marquardt, Mary J. Packard, Owen J. Sexton, Allen Vinegar, and Bruce A. Wunder for their
careful readings of drafts of this article. Carol Roth worked tirelessly preparing sectionsof lizard eggs for
study by light microscopy, and Charles Vassbrinck and William Rubink provided invaluable assistance
with electron microscopy. Special thanks go to the personnel of the William Morgan Library at Colorado
State University who filled our seemingly endless requests for interlibrary loan of critical research
materials. Drafts of the manuscript were expertly typed by Kirby Maxwell and Reta Herbertson. Our
labours were supported, in part, by the Department of Zoology and Entomology at Colorado State
University, and by grants from the National Science Foundation (Number DEB 75-18179 to G. C.
Packard) and the National Institutes of Health (Number NS 12257 to C. L. Ralph).
I01
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Biol. Rm . (1977). 52. p p 71-105

THE PHYSIOLOGICAL ECOLOGY OF REPTILIAN

BY GARY C PACKARD. C. RICHARD TRACY AND JAN J . ROTH

HZgher levels of classifiation of surviving members of the

depends as much upon adaptations of embryonic stages as upon adaptations of adults,

Oviparity presumably represents the ancestral mode of reproduction in the Class

Physiological ecology of reptilian embryos

Physiological ecology of reptilian embryos

(I) Uptake of water from soil

Physiological ecology of reptilian embryos

(b) Calcareous eggs

volume of albumen, in contrast to eggs of other squamate reptiles, or whether water

Mechanism of water transport into eggs

where me = water uptake by the egg (g.min-l), (Ysoil

Physiological ecology of reptilian embryos

Conversely, consideration of the physical determinants of water transport reveals the

Fig. 3. Cumulative plots of nitrogen excreted as ammonia (A), urea (0)

Physiological ecology of reptilian embryos

(3) Adaptive szjpificance of water uptake

Physiological ecology of reptilian embryos

Fig. 4. Cumulative plots of nitrogen excreted as ammonia (A), urea (0)

Fig. 5. Cumulative plots of nitrogen excreted as ammonia (A), urea (0)

Physiological ecology of reptilian embryos

The pattern of nitrogen excretion manifest by embryos of the alligator, Alligator

protein catabolism has important implications concerning the water metabolism of

(I) The atmosphere adjacent to eggs

(2) The mechanism of gas exchange

Physiological ecology of reptilian embryos

(I) Effects of temperature

Physiological ecology of reptilian embryos

Summary of the modes of reproduction characterizing families of

investigators to detect an inflection point in plots of oxygen consumption against age

Distribution of the live-bearing method

Physiological ecology of reptilian embryos

Data summarized in Table z indicate that viviparity has arisen independently in

model for the evolution of viviparity

Physiological ecology of reptilian embryos

(3) Adaptive value of egg retention

Physiological ecology of reptilian embryos

of those embryos in the relatively favourable thermal environment afforded by the

(b) Waterfor embryonic development

Physiological ecology of reptilian embryos

reduction in shell thickness that is required if intra-uterine development is to proceed

(c) Food for emergent young

( d ) Protection of developing embryos

(e) Arboreal and aquatic habits of adults

Physiological ecology of reptilian embryos

( 5 ) Why are there no viviparous turtles or crocodilians?

Physiological ecology of reptilian embryos

Physiological ecology of reptilian embryos

LYNN,W. G. & ULLRICH,Sister M. C. (1950). Experimental production of shell abnormalities in

Physiological ecology of reptilian embryos

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