350 REPROOUCTIVE BIOLOGY AND EMBRYOLOGY OF CROCODILIANS b!l OJ I-< shelled eggs are stored longer than <strong>the</strong> last. However, <strong>the</strong>y all appear to be ..c OJ 'O.S .... 0 ~ ~ c"1:S III en Lf) N c OJ at comparable stages <strong>of</strong> development at <strong>the</strong> time <strong>of</strong> laying (see Section VI). If': .- III 0... 0'"-< £! 6 '" .-< .-< o .-< When first laid, <strong>the</strong> eggs are coated with a slimy gel (Goodwin <strong>and</strong> Marion, i3b c .... 0 +1 ~ "' N ..... 1 'y; til 00» +1 +1 +1 500 1978). On average, 3 to 15% <strong>of</strong> eggshells are cracked during <strong>the</strong> laying "" t ~u::;a15..c: o Lf) Lf) .-< Ei x .~ o OJ 0 >"'~6.B I-< I-< process (Joanen, 1969; Pooley, 1969a; Webb et al., 1977; Goodwin <strong>and</strong> -< ~ ~..2 ::l D .~ ~ u D Marion, 1978). Cracked eggs develop normally if <strong>the</strong> shell membrane re 'J> 'J> OJ~ '" '" 'y; mains intact, but if it is torn, <strong>the</strong> eggs rot or are eaten by ants (Joanen, 1969; Ei '" 'J> OJ .~ '" Ei..c Goodwin <strong>and</strong> Marion, 1978). The number <strong>of</strong> eggs present in each nest If) r--.. o ~ If': .. ~ {3 0 ọ I-< ::l -< c:i o '"--l III ~ 0 ~en -- '"d ....... I:Q Ei ;; > "8 '[ Ei _ ("lj lr) maternal age <strong>and</strong> clutch size, egg size, <strong>and</strong> egg quality in Alligator mississip ., -< piensis (Table IV). "Middle-aged" females are obViously <strong>the</strong> most "success QI ~~~ 00 'w;:n "0 ONe ful" breeders in terms <strong>of</strong> both quantity, size, <strong>and</strong> quality <strong>of</strong> <strong>the</strong> eggs pro 00 6 ~ -O~00 '" ;::J CJ duced. Interestingly, old females are nearly as successful, although <strong>the</strong>ir '1:l 6..c: C· ..... -£ ~ ..0 C .- 'w Lf) clutch size is usually smaller <strong>and</strong> more malformed embryos result, whereas III Ei § c ~ 6 0 N ;:l ..... "O"'~ ~ -< '" Z 0 ~ +1 'D o .5 N ~ N OJ OJ '" males (which may mate with ei<strong>the</strong>r large or small males). Similar relation 0... '" c w "" a ~ '" I:I.. til W"'"O season. 15 ~ '" ~ I ;:l 6"1:S ~ gg c o~ bO~~_'""Ol-log OJ OJ '" For several species, weight <strong>of</strong> eggs correlates positively with that <strong>of</strong> §~:g~8..8:;c ~ &3 ~:< eno .- ro 0-,; bJ ........ rc hatchlings (Staton <strong>and</strong> Dixon, 1977; Deitz <strong>and</strong> Hines, 1980; Webb et al., E5 gg >
3152 REPROOUCTIVE BIOLOGY AND EMBRYOLOGY OF CROCODILIANS 1983b, e). In mammals, fetuses with a low birth weight are frequently malformed, <strong>and</strong> <strong>the</strong> same is true <strong>of</strong> <strong>the</strong> small light eggs laid by young female alligators (Table IV). The alligator is an excellent animal model in which to study such malformations. The eggs <strong>of</strong> middle-aged females are also useful for teratogenic studies as <strong>the</strong>y show a lower basal incidence <strong>of</strong> spontaneous malformations than avian eggs (Ferguson, 1981a). Possible factors that determine <strong>the</strong> relationships <strong>of</strong> egg fertility <strong>and</strong> rate <strong>of</strong> embryonic malformation with maternal age include <strong>the</strong> following: (1) reduced ovulation <strong>of</strong> young <strong>and</strong> old females, (2) <strong>the</strong> immaturity <strong>of</strong> young ova, (3) slight asynchrony between <strong>the</strong> times <strong>of</strong> ovulation <strong>and</strong> copulation in young females, (4) <strong>the</strong> lower sperm numbers <strong>and</strong> quality in males near <strong>the</strong> end <strong>of</strong> <strong>the</strong> breeding cycle (when young females mate), <strong>and</strong> (5) <strong>the</strong> poorer quality <strong>of</strong> <strong>the</strong> large ova released by old females. There is some evidence that prior to senescence old females ei<strong>the</strong>r resorb <strong>the</strong>ir ova or <strong>the</strong>ir eggs, or both. Possibly, young <strong>and</strong> very old females contribute little to population recruitment. Nest temperature <strong>and</strong> humidity are important factors for embryonic survival, development, growth, <strong>and</strong> sex determination (Table III). Only Alligator mississippiensis (McIlhenny, 1934, 1935; Joanen, 1969; Chabreck, 1973), Crocodylus porosus (Webb, 1977a; Webb et a1., 1977, 1983b; Magnusson, 1979c), Caiman crocodilus (Staton <strong>and</strong> Dixon, 1977) <strong>and</strong> Crocodylus acutus (Lutz <strong>and</strong> Dunbar Cooper, 1982, 1984) have been studied in detail. In general, <strong>the</strong> positioning <strong>and</strong> construction <strong>of</strong> nests ensure fairly stable <strong>the</strong>rmal <strong>and</strong> humidity conditions within <strong>the</strong> egg cavity. Crocodilian nests may obtain three sources <strong>of</strong> heat: solar heating, decomposition, <strong>and</strong> metabolism. The temperature <strong>of</strong> <strong>the</strong> nest cavity is equilibrated; <strong>the</strong> outer layers <strong>of</strong> <strong>the</strong> nest absorb solar heat at times <strong>of</strong> maximum incidence, but slow its passage to <strong>the</strong> central cavity; some <strong>of</strong> this heat later dissipates to <strong>the</strong> central cavity. However, solar energy is unlikely to be <strong>the</strong> sole source <strong>of</strong> heat, as crocodilian mean nest temperatures are <strong>of</strong>ten 1° to 5°C above <strong>the</strong> mean air temperature (McIlhenny, 1935; Joanen, 1969; Chabreck, 1973; Modha, 1967; Webb et a1., 1977, 1983b; Staton <strong>and</strong> Dixon, 1977). The temperature <strong>of</strong> mound nests may be raised by <strong>the</strong> decomposition <strong>of</strong> <strong>the</strong> nesting vegetation, particularly during <strong>the</strong> early stages <strong>of</strong> incubation (McIlhenny, 1935; Joanen, 1969; Chabreck, 1973; Webb et a1., 1977a, 1983b; Staton <strong>and</strong> Dixon, 1977; Magnusson, 1979c). Such decomposition may be enhanced by females urinating onto <strong>the</strong> nest during <strong>and</strong> after its construction (Pooley, 1962, 1969a, b; Chabreck, 1975; McIlhenny, 1934, 1935; Reese, 1915a; Deraniyagala, 1936, 1939; Whitaker <strong>and</strong> Whitaker, 1976b, 1977b; Tryon, 1980; Webb et a1., 1983b). However, decomposition should be minimal during <strong>the</strong> latter stages <strong>of</strong> incubation in mound nests <strong>and</strong> nonexistent in hole nests. Embryonic metabolism has also been postulated to represent a source <strong>of</strong> heat (Modha, 1967; Magnusson, 1979c; Webb et a1., 1983b). Clearly, <strong>the</strong> extent <strong>of</strong> such heating varies with <strong>the</strong> proportion <strong>of</strong> <strong>the</strong> REPRODUCTIVE BIOLOGY 3153 dutch containing living embryos. The assumption (Staton <strong>and</strong> Dixon, 1977; Webb et a1., 1983b) that <strong>the</strong> rate <strong>of</strong> heating increases up to <strong>the</strong> end <strong>of</strong> incubation implies that heating relates more closely to <strong>the</strong> size <strong>of</strong> <strong>the</strong> embryo (Drent, 1967) than to its metabolic rate. Indeed, <strong>the</strong> peak weightspecific metabolic rate in C. porosus occurs during <strong>the</strong> period <strong>of</strong> <strong>org</strong>anogenesis (i.e., during early/middle incubation; G. Grigg, personal communication). This assumption correlates with <strong>the</strong> fact that nests <strong>of</strong> A. mississippiensis are <strong>of</strong>ten warmer during <strong>the</strong> second to fourth week <strong>of</strong> incubation than later in <strong>the</strong>ir 9-week incubation period (Chabreck, 1973). Moreover <strong>the</strong> hole nests <strong>of</strong> C. acutus (Lutz <strong>and</strong> Dunbar Cooper, 1982, 1983) <strong>and</strong> C. joJmsoni (Webb <strong>and</strong> Smith, 1984) become progressively warmer during incubation, <strong>and</strong> this temperature rise may accelerate development <strong>and</strong> improve survivorship (Webb <strong>and</strong> Smith, 1984). Although critical for successful embryonic development, nest humidity <strong>and</strong> <strong>the</strong> water relations <strong>of</strong> crocodilian eggs are poorly understood. ,All crocodilian nests studied to date have exhibited very high humidities (Table III). Precise data on <strong>the</strong> mechanisms <strong>of</strong> humidity maintenance are lacking, but <strong>the</strong>re have been reports <strong>of</strong> maternal behavior involving urination <strong>and</strong> splashing <strong>of</strong> <strong>the</strong> nest (e.g., Whitaker <strong>and</strong> Whitaker, 1976b, 1977b). If this is deliberate, it would imply that <strong>the</strong> mo<strong>the</strong>r can monitor nest temperature <strong>and</strong>/or humidity, <strong>and</strong> it has been suggested that this might be <strong>the</strong> function <strong>of</strong> sensory receptors on <strong>the</strong> jaws (Ferguson, 1979b, 1981b, 1982b; see also Section II.E). However, during abnormally hot dry years, <strong>the</strong> humidity within nests <strong>of</strong> A. mississippiensis decreases, <strong>and</strong> <strong>the</strong> eggs begin to form abnormal air spaces (Ferguson <strong>and</strong> Joanen, 1983) due to cleavage <strong>of</strong> <strong>the</strong> shell membrane away from <strong>the</strong> calcified eggshell. If <strong>the</strong> air space is large, it causes embryonic death, representing a significant source <strong>of</strong> mortality, particularly among eggs near <strong>the</strong> top <strong>of</strong> alligator nests during hot dry years. Nest temperatures <strong>and</strong> humidities outside <strong>the</strong> normal range lead to malformed or dead embryos (Modha, 1967; Bustard, 1969, 1980a, c; Pooley, 1962, 1969a, h; Whitaker <strong>and</strong> Whitaker, 1976a, b, 1977b; Joanen <strong>and</strong> McNease, 1975a, b, 1977, 1979a, 1980, 1981; Staton <strong>and</strong> Dixon, 1977; Ogden, 1978; Ferguson <strong>and</strong> Joanen, 1983; Webb et a1., 1983a,b,e). Within <strong>the</strong> range <strong>of</strong> viable temperatures, temperature <strong>and</strong> incubation time are inversely correlated (Reese, 1915a; McIlhenny, 1934, 1935; Pooley, 1962, 1969a,b; Joanen <strong>and</strong> McNease, 1975a, b, 1977, 1979a, 1980; Packard et a1., 1977; Webb et a1., 1977, 1983a,b,e; Ferguson, 1982b; Ferguson <strong>and</strong> Joanen, 1982, 1983). Thus, <strong>the</strong>re are only mean incubation periods (Table III), <strong>and</strong> field incubation times are difficult to interpret even with scant information on nest temperatures. Consequently, developmental stages must be related to an arbitrary (normal) time scale calculated for controlled environmental conditions (Ferguson, 1982b; Webb et a1., 1983a). The gaseous conditions within crocodilian nests have been assayed twice, once for <strong>the</strong> hole nests <strong>of</strong> Crocodylus acutus (Lutz <strong>and</strong> Dunbar
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