Reproductive Biology and Embryology of the ... - Seaturtle.org

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REPRODUCTIVE alOLOGY ANO EMBRYOLOGY OF CROCODILIANS
there is no internal pipping, as seen in birds (Rahn et a1., 1979). Hence,
crocodilian hatchlings are unlikely to breathe until the shell and membranes
are broken and the flUids are drained from around the head. The
time interval between this event and emergence from the egg is relatively
short (ranging from a few minutes to 24 hours), so that the transition from
chorioallantoic to pulmonary respiration must be rapid, as in mammals
and megapode birds (Seymour and Ackerman, 1980), but it is contrary to
the slow transition in other birds (Rahn et a1., 1979). Details of this transition
(e.g., the extent of chorioallantoic perfusion during the time between
first breathing and hatching) are unknown but of considerable interest.
The problem is even more intriguing when one recalls that for many hours
prior to pipping embryos vocalize in response to certain stimuli (see Section
11.E); this suggests that the lungs are functional during this period. As
alligator eggs progressively lose water during incubation, an air bubble
forms beneath the shell membrane and this moves around in the albumen,
so as to always lie beneath the uppermost surface of the egg (Ferguson,
1982a): similar events OCCur in megapode eggs (Seymour and Ackerman,
1980). Perhaps this air is used prior to pipping (analogous to the internal
pipping of avian embryos). This area is significant because late embryonic
death is common (during both natural and artificial incubation) and could
be caused by improper hydric conditions. Thus, high humidity may be
required during the early stages of incubation, but lower humidity may be
reqUired during the later stages to facilitate water loss and the formation of
intra-egg air. This in turn may enable internal breathing, the maturation of
the respiratory system, and provide the extra oxygen required for pipping.
Indeed, Vocalization may represent a signal that the embryo is mature
enough to survive outside the egg, and it remains to be determined
whether it occurs in eggs incubated under conditions of continuous high
humidity. The changing hydric conditions are likely to be most critical in
species with long incubation periods (e.g., Crocodylus porosus).
During the hatching process, the embryo first widens the slit in the shell
membrane (frequently by pushing its snout into the slit and then opening
its jaws). Second, it pUShes out the entire head and neck; after a couple of
minutes, one quick forceful thrust forces the whole bOdy out of the egg
(Fig. 4). The claws may be used in the hatching process. The ruptured
extraembryonic membranes progressively detach from the shell membrane
but remain attached to the umbilical region of the hatchling for about a day;
they eventually shrivel, dry up, and break (Fig. 21). Hatchlings are COvered
with slime, presumably derived from the ruptured allantois, and they
smell of ammonia. This slime dries after about 24 hours. At the time of
hatching, the abdomen is distended by absorbed yolk and the umbilical
car is evident (Fig. 21). The yolk serves as a food supply for a few weeks
ntil the hatchlings begin feeding so that the abdomen becomes less dis­
~ended and the umbilicus closes. In hatchlings kept below 210C, the umilicus
does not heal correctly, yolk is not utilized, and the animals usually
e (King and Dobbs, 1975).
THE EGGSHELL AND SHELL MEMBRANES
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The precise hatching trigger remains unknown. Mechanical stimuli and
vocalizations may playa role (see Section II.E). Growth and movement of
the embryo may burst the shell. Increasing levels of waste products, decreasing
egg water, and the progressive inadequacy of gas exchange may
also stimulate hatching. Temperature seems to be important; field reports
note that an inadvertent rise in egg temperature stimulates premature
hatching, and, conversely, decreases in egg temperature delay hatching
(McIlhenny, 1934, 1935; Deraniyagala, 1936, 1939; Pooley, 1962, 1969a,
1971). Hatchlings are sufficiently well developed to be viable if they hatch
several days prematurely (McIlhenny, 1934, 1935) so that completion of
development is not the final trigger for hatching. Lengths and weights of
the hatchlings from different species are summarized in Table III.
III.
THE EGGSHELL AND SHELL MEMBRANES
A. General
Most crocodilian eggs are elliptical with approximately equivalent ends
(Figs. 5A to 1). They vary considerably in size and shape, even within
species (Tables III and IV). Normally there is little variation in size and
shape within an individual clutch. However, occasional large, infertile,
double-yolked eggs or very small eggs are seen; these abnormal eggs are
usually laid at the beginning and end of oviposition and are common in
clutches laid by young females (Ferguson and Joanen, 1983). Ferguson
(1982a) described the structure and composition of the eggshell and shell
membranes of Alligator mississippiensis and provided a comprehensive review
of the literature.
B. Egg Banding
The gradual development of a transverse white band across fertile crocodilian
eggs has been known for nearly a century (Clarke, 1888a,b, 1891),
and reports are now available for several species (Ferguson, 1982a; Reese,
1908, 1912, 1915a, 1931a; McIlhenny, 1935; Deraniyagala, 1936, 1939; Webb
et aI., 1977, 1983a, b, e; Webb, 1977a; Beck, 1978; Hara and Kikuchi, 1978;
Deitz and Hines, 1980; Tryon, 1980).
Within 24 hours of egg laying, the eggs of Alligator mississippiensis show
a small opaque, chalky white, oval patch on their top surface (Figs. 5A and
6). The small embryo has attached itself to the innermost surface of the
shell membrane immediately below this opaque patch. At this and all
subsequent stages, the white color is associated with changes both of the
eggshell and shell membrane (which itself appears chalky white in this
area). Initially the oval opaque patch expands in width around the shell,
extending approximately half-way around the shell on days 3 to 4, threequarters
way around the shell on days 5 and 6, and completely around the