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Resorption of Oviductal Eggs and Embryos in Squamate Reptiles

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Resorption of Oviductal Eggs and Embryos in Squamate Reptiles HERPETOLOGICAL JOURNAL, Vol. 8, pp. 65-71 ( 1998) RESORPTION OF OVIDUCTAL EGGS AND EMBRYOS IN SQUAMATE REPTILES DANIEL G. BLACKBURN Department of Biology, Life Sciences Center, Tr inity College, Hartford, CT 06106, USA Among squamate reptiles, gravid females are frequently said to be able to resorb infertile and malformed eggs from their oviducts. This pattern, if it existed, would allow females to recycle nutrients from abortive attempts at reproduction, and to increase lifetime reproductive potential by modulating reproductive effort according to environmental circumstances. However, . a review of the literature reveals that evidence for oviductal egg resorption is weak, and does not preclude other fates for abortive eggs (egg retention or expulsion). Furthermore, for the oviduct to resorb eggs would require that it have the fu nctional properties of the digestive tract, properties that may be incompatible with its several reproductive fu nctions. Future work should not assume oviductal egg resorption in squamates without definitive evidence that the eggs are not simply aborted or retained by fe males following absorption of water. INTRODUCTION 1970a; Thompson, 1977, 1982; Stewart, 1989; Stewart et In literature dating back to the late 1800s, fe male liz­ al., 1990). However, as shown by these and other ards and snakes have been said to be able to resorb eggs studies (Thompson, 1981; Stewart & Castillo, 1984), and embryos from their oviducts under conditions of the yolk typically provides most of the nutrients for de­ physiological stress and infertility. Theoretically, such velopment. Therefore, given that most of female resorption could be an ideal way fora fe male to mini­ nutrient investment into the prospective neonate occurs mize loss of nutrients during failed attempts at at the time of ovulation in both oviparous and vivipa­ forms, a female that could resorb the yolk or the reproduction, and to control reproduction in such a way rous as to maximize lifetime reproductive potential. How­ developing embryo could achieve considerable savings ever, as discussed below, evidence for resorption is of energy and nutrients. weak, and several reasons exist to question whether A second potential advantage of egg resorption is specific squamates actually resorb oviductal eggs, as that it would allow females to minimize the physical opposed to aborting them. The purpose of this review is burden imposed by inviable eggs. Gravidity tends to to explore the question of whether squamates can handicap locomotory ability in femalesquamates (e.g., et resorb their eggs and embryos, and to encourage indi­ Vitt & Congdon, 1978; Shine, 1980; Seigel al., 1987; et et viduals with experience in herpetoculture to sbare Cooper al., 1990; Sinervo al., 1991; also see evidence bearing on egg resorption in particular spe­ Schwarzkopf, 1993). Moreover, in some snake species, cies. Th is issue is of functional, theoretical, and females do not fe ed during pregnancy (Shine, 1980), evolutionary significance, and has practical implica­ probably because gravidity inhibits passage of food tions for the maintenance and breeding ofsquamates in down the posterior gastrointestinal tract. Therefore,by captivity. carrying a clutch of inviable eggs, a female would be decreasing her ability to fe ed, thermoregulate, and es­ THEORETICAL ADVANTAGES OF EGG cape from predators, with no compensatory RESORPTION advantages. An ability to resorb eggs and embryos could offe r Thirdly, inviable eggs block the oviducts and would important benefits to female squamates. In typical prevent future attempts at reproduction if not removed. oviparous squamates, the developing eggs spend about The squamate uterus is a thin tube that, in repose, is 20-40% of the total developmental period in the much smaller in diameter than a single egg. An egg oviducts, prior to being laid (Shine, 1983; Blackburn, lodged in the uterus could block eggs from subsequent 1995). Therefore, an opportunity for resorption could ovulations from being transported through the exist in egg-layers, as well as in viviparous forms, oviducts, and might well prevent sperm from ascending which retain their eggs to term. By resorbing infertile the tract to the site of fertilization. Resorption of invi­ and malformedeggs, a female could recycle the nutri­ able eggs would be an ideal way for femalesto free up ents that she has invested in her eggs, and thereby the oviducts for subsequent reproductive attempts. enhance her own future survival and reproduction. In A fourth potential benefit of egg resorption comes oviparous squamates, most or all of the nutrients in­ from consideration of life history theory (Stearns, vested into eggs are in the fo rm of the ovulated yolk, 1992). If a female could resorb eggs under conditions and a similar situation exists in most live-bearing spe­ of physiological stress, she could modulate reproduc­ cies. In viviparous lizards and snakes, small amounts of tion after ovulation, according to changing organic and inorganic ions are provided to the embryos environmental circumstances. If conditions were un­ by the oviduct afterovulation (Panigel, 1956; Hoffman, suitable (or simply less than ideal) forreproduction, a 66 D. G. BLACKBURN female could resorb her reproductive investment and contained oviductal embryos and adnexae that had wait until conditions improved to reproduce. Unsuit­ been retained fromthe preceding summer. This also oc­ able conditions could be reflected in unseasonal curs in oviparous species. For example, a fe male climatic change, depletion of maternal fat reserves, or Diadophis was reported to retain a fertilized, dead egg foodscarcity. A viviparous female that could not resorb for some months (Blanchard, 1925), and a fe male or otherwise get rid of her eggs would be "locked in" to Elaphe climacophora reportedly retained an oviductal pregnancy, carrying the embryos until they were finally egg formore than 16 months (Watanabe et al., 1989). born,even at the expense of her own survival. This con­ Thus, inviable eggs may be retained in the oviducts, sideration may be less significantfor typical oviparous rather than being actively resorbed, even though such squamates; given the smaller proportion of the devel­ retention may have detrimental affects on subsequent opmental period that eggs reside in the oviducts, the reproduction. opportunity for fe males to modulate reproductive in­ Alternatively, malformed or infertile eggs could vestment after ovulation would necessarily be less than eventually be expelled by the oviducts and extruded via in viviparous forms. In the latter, gestation length the cloaca. Squamates are routinely reported to deposit ranges from several weeks to about a year, depending infertile and abnormal eggs, including both oviparous on the species (Tinkle & Gibbons, 1977; Blackburn & species (e.g., Rollinat, 1904; Neill & Boyles, 1957; Vitt, 1992); therefore, environmental conditions could Fitch, 1970; Campbell & Quinn, 1975; Dyrkacz, 1977; change markedly between the period of ovulation and Murphy et al., 1978) and viviparous species (Jacobi, parturition. Consequently, from this standpoint, we 1936; Branch, 1973; Branson & Baker, 1974; Mitchell, would expect the capability of egg and embryo 1976; Ji, 1995; Ronne, 1996). For example, a captive resorption to be particularly advantageous to vivipa­ Elaphe longissima female wasobserved to deposit invi­ rous species. able, deformed eggs of subnormal size; the eggs were not laid as a clutch, but extruded at the rate of one or DO FEMALE SQUAMA TES RESORB two a day as the snake crawled around the cage OVIDUCTAL EGGS? (Lotzke, 1975). In an analysis of 162 Thamnophis An ability to resorb eggs while they are still in the sirtalis that had been captured and then maintained in oviducts clearly could have important advantages for captivity, Gregory et al. (1992) found that about a quar­ fe male squamates. The question remains, however, as ter of the deposited litters included fu lly-developed but to whether females are able to accomplish such dead young; another quarter contained one or more un­ resorption. Uterine resorption of embryos is well developed eggs or young. Interestingly, snout vent known to occur among eutherian mammals, notably length of the live and dead neonates did not differ sta­ certain rodents (Brambell, 1948; Macfarlane et al. , tistically. Data reported by Ji (1995) on the viviparous 1957; Low, 1978; Gosling, 1986; Westlin et al., 1995). E. rufodorsata indicate that infertile eggs extruded at However, evidence for egg resorption among the end of gestation do not differ from oviductal eggs squamates is less clear. collected months earlier, in terms of lipid content or ca­ Uterine egg resorption has been inferred for particu­ loric value. One would expect a decline in both lar species of both lizards and snakes (e.g., Mingazzini, parameters if organic components were being resorbed. 1892; Domini, 1928; Jacobi, 1936; Clausen, 1940; As anyone with experience with captive breeding of Kasturirangan, 1951; Parameswaran, 1962; Bustard, viviparous squamates knows, extrusion of inviable 1966; Hoffm an, 1970b; Yaron, 1972), based on three eggs occurs with great frequency; to breeders they are separate lines of evidence. First, such inferences some­ known as "slugs''. In my laboratory, we have frequently times are based on observations of oviductal eggs that observed extruded yolky material in the sandy substrate have stopped developing, or that show no evidence of in my breeding colony of Chalcides
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