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

35B
REPROOUCTIVE BIOLOGY ANO EMBRYOLOGY OF' CROCODILIANS
REPRODUCTIVE BIOLOGY
3551
following: (1) Reduction of losses from predation, flooding, or physical
damage to the nest (e.g., by another nesting crocodile); (2) control and
optimization of the incubation environment; (3) control of the sex and
possibly the future growth of hatchlings (Ferguson and Joanen, 1982,
1983); (4) monitoring development by observing changes in eggshell banding
(see Section III. B) and detecting (in order to discard) infertile,
malformed, dead, or infected eggs; (5) acceleration or delay of development
by altering the incubation temperature and synchronization of hatchling
emergence; (6) correction of the orientation of eggs laid in a detrimental
position. Thus embryos of eggs laid upright (i.e., with their long axes at
right angles to the nest base) frequently die or are malformed; they develop
normally if the eggs are reoriented so that the embryonic disk becomes
positioned beneath the top center of the egg.
The death of embryos following egg inversion may explain why viviparity
never evolved in the Crocodilia or Testudines. During the evolution of
viviparity, there is usually an intermediate stage in which the embryo
develops inside an egg retained within the oviducts of the female. However,
in taxa in which the embryo attaches to the shell membrane and
turning or inversion result in embryonic death, this intermediate stage is
unlikely to be achieved. The absence of crocodilian viviparity may also be
related to increased dependence of embryos on eggshell calcium as compared
to the very slight dependence of snakes and lizards (Packard et aI.,
1977), the absence of biological advantages for prolonged egg retention,
and the evolution of nest guarding (Tinkle and Gibbons, 1977).
Artificial incubation of the eggs of "hole nesters" has been effected by
reburying the eggs in suitable sites (Pooley, 1969a, b, 1971; Blake and
Loveridge, 1975; Bustard, 1980c). Earlier attempts at incubating the eggs of
mound nesters, e.g., Alligator mississippiensis, involved placing them in
buckets of nesting material maintained at the appropriate temperature and
humidity (Reese, 1901a, 1931a; Table III). Currently eggs are incubated
either in incubators or in environmental chambers (Joanen and McNease,
1974a,b, 1976, 1977, 1979a, 1980, 1981). Tests relating to the incubation of
alligator eggs, including stacked versus nonstacked, wild eggs versus eggs
from captive breeding programs, oxygenated chambers versus nonoxygenated
chambers, washed eggs versus nonwashed eggs, exposed eggs
versus eggs covered with nesting material, and eggs set over water versus
eggs set over dry concrete (Joanen and McNease, 1977) showed no appreciable
effects, except for a 13% decrease in hatching success from stacked
eggs, and a lower hatching rate (72%) for captive produced eggs than for
those of wild animals (94%). About 15% of embryos from captive produced
eggs died around hatching, and others had to be assisted from the shell
(Joanen and McNease, 1975a, 1977). This may indicate weakness of the
hatchling (compacted yolks are more common in this group) or abnormal
toughness of the eggshell and its membranes. Decreased hatching success
in farmed turtles may be associated with replacement of the normal arago-
nite crystals of calcium carbonate by calcite crystals (Solomon and Baird,
1979; Baird and Solomon, 1979). Although the eggshells of farmed crocodilians
may be defective, it seems more likely that decreased fecundity and
increased abnormality may result from maternal dietary deficiencies, e.g.,
that of vitamin E (Lance, 1982; Lance et a!., 1983; Elsey and Lance, 1983) or
inappropriate husbandry (Joanen and McNease, 1981; Lance, 1984).
Incubation of alligator eggs at temperatures ranging from 26° to 34°C,
produces the best hatching success at 30° to 32°C (Joanen and McNease,
1977, 1979a, 1980, 1981; Ferguson and Joanen, 1982, 1983). Hatchlings from
eggs incubated below 28°C often twitch, have balance difficulties and swim
with their heads constantly under water; eventually they drown. Eggs of
Crocodylus novaeguineae incubated at 23°, 26°, and 38°C (normal approximately
32°C) have a low hatching success (Bustard, 1969, 1971). All survivors
of the high temperature group showed tail and other abnormalities
and had to be helped from their shell. Hatchlings of C. palustris recovered
from overheated nests also showed tail abnormalities (Whitaker and
Whitaker, 1976a,b).
Crocodilian eggs are susceptible to changes in humidity; at low levels
the shell membrane dries out and shrivels, thereby killing the embryo
(McIlhenny, 1935; Deraniyagala, 1939; Pooley, 1962, 1969a, b, 1971; Joanen,
1969; Staton and Dixon, 1977). The optimum relative humidities for incubating
Alligator mississippiensis eggs is 90 to 92% (Joanen and McNease,
1977, 1979a; Chabreck, 1975). Abnormal air spaces form in alligator eggs
incubated at suboptimal humidities (Ferguson and Joanen, 1983); large air
spaces are lethal. Intact eggs of Crocodylus acutus are resistant to desiccation,
losing water at a rate comparable to the eggs of birds (Rahn and Ar,
1974; Rahn et aI., 1979; Ar and Rahn, 1980; Diamond, 1982), but at a rate
much lower than that of the leathery-shelled eggs of Iguana iguana (Rand,
1968). Removal of a 3 x 3 cm piece of shell (leaving the shell membrane
intact) from the eggs of C. acutus greatly increases the desiccation rate
(Rand, 1968). The eggs of C. novaeguineae apparently could either lose or
gain up to 25% water with no adverse effects on the embryos (Bustard,
1971). The soft-shelled eggs of many squamates and turtles can adsorb
(and then lose) water up to 300% of their initial weight (Bustard, 1971;
Packard et aI., 1977); unlike the eggs of crocodilians (and certain other
turtles) they lack large quantities of hydrophilic albumen, which are likely
to reduce the rate of water loss under adverse conditions.
Bustard (1971) has suggested that water uptake is unessential in crocodilian
eggs, but represents an insurance against lethal levels of water stress
caused by possible adverse environmental conditions later in development.
However, Packard et al. (1977) reported that water uptake was critical
for normal reptilian embryonic development; prevention of water uptake,
particularly in the early stages of incubation, leads to high rates of
mortality and developmental abnormalities. Indeed, Tracy et a!. (1978)
suggested that the only major difference between the eggs of birds and