The Evolutionary Economics of Embryonic-Sac Fluids in Squamate Reptiles.

The parchment-shelled eggs of squamate reptiles take up substantial water from the nest environment, enabling the conversion of yolk into neonatal tissue and buffering the embryo against the possibility of subsequent dry weather. During development, increasing amounts of water are stored in the embryonic sacs (i.e., membranes around the embryo: amnion, allantois, and chorion). The evolution of viviparity (prolonged uterine retention of developing embryos) means that embryonic-sac fluid storage now imposes a cost (increased maternal burdening), confers less benefit (because the mother buffers fetal water balance), and introduces a potential conflict among uterine siblings (for access to finite water supplies). Our data on nine species of squamate reptiles and published information on three species show that the embryonic-sac fluids comprise around 33% of neonatal mass in viviparous species versus 94% in full-term eggs of oviparous squamates. Data on parturition in 149 vipers (Vipera aspis, a viviparous species) show that larger offspring store more fluids in their fetal sacs and that an increase in litter size is associated with a decrease in fluid-sac mass per offspring. Overall, the evolutionary transition from oviparity to viviparity may have substantially altered selective forces on offspring packaging and created competition among offspring for access to water reserves during embryonic development.

Thermal strategies and energetics in two sympatric colubrid snakes with contrasted exposure.

The thermoregulatory strategy of reptiles should be optimal if ecological costs (predation risk and time devoted to thermoregulation) are minimized while physiological benefits (performance efficiency and energy gain) are maximized. However, depending on the exact shape of the cost and benefit curves, different thermoregulatory optima may exist, even between sympatric species. We studied thermoregulation in two coexisting colubrid snakes, the European whipsnake (Hierophis viridiflavus, Lacépède 1789) and the Aesculapian snake (Zamenis longissimus, Laurenti 1768) that diverge markedly in their exposure, but otherwise share major ecological and morphological traits. The exposed species (H. viridiflavus) selected higher body temperatures (approximately 30 degrees C) than the secretive species (Z. longissimus, approximately 25 degrees C) both in a laboratory thermal gradient and in the field. Moreover, this difference in body temperature was maintained under thermophilic physiological states such as digestion and molting. Physiological and locomotory performances were optimized at higher temperatures in H. viridiflavus compared to Z. longissimus, as predicted by the thermal coadaptation hypothesis. Metabolic and energetic measurements indicated that energy requirements are at least twice higher in H. viridiflavus than in Z. longissimus. The contrasted sets of coadapted traits between H. viridiflavus and Z. longissimus appear to be adaptive correlates of their exposure strategies.

Gestation, thermoregulation, and metabolism in a viviparous snake, Vipera aspis: evidence for fecundity-independent costs.

Oxygen consumption of gestating Aspic vipers, Vipera aspis (L.), was strongly dependent on body temperature and mass. Temperature-controlled, mass-independent oxygen consumption did not differ between pregnant and nonpregnant females. Maternal metabolism was not influenced during early gestation by the number of embryos carried but was weakly influenced during late gestation. These results differ from previous investigations that show an increase in mass-independent oxygen consumption in reproductive females relative to nonreproductive females and a positive relationship between metabolism and litter size. These data also conflict with published field data on V. aspis that show a strong metabolic cost associated with reproduction. We propose that, under controlled conditions (i.e., females exposed to precise ambient temperatures), following the mobilisation of resources to create follicles (i.e., vitellogenesis), early gestation per se may not be an energetically expensive period in reproduction. However, under natural conditions, the metabolic rate of reproductive females is strongly increased by a shift in thermal ecology (higher body temperature and longer basking periods), enabling pregnant females to accelerate the process of gestation. Combining both laboratory and field investigation in a viviparous snake, we suggest that reproduction entails discrete changes in the thermal ecology of females to provide optimal temperatures to the embryos, whatever their number. This results in the counterintuitive notion that metabolism may well be largely independent of fecundity during gestation, at least in an ectothermic reptile.

Body condition threshold for breeding in a viviparous snake.

One major goal of physiological ecology is to seek links between life history traits. Identification of a body condition threshold for breeding (e.g. critical level of body reserves) provides a link between the physiological process involved in storage of body reserves and the ability to reproduce. One hundred and twenty-nine freeranging adult female Vipera aspis, a viviparous snake, were marked with electronic identification tags and/or by scale clipping, weighed, and measured at the onset of vitellogenesis, and immediately released in the field in western central France (47°03'N; 02°00'W). The 129 snakes were recaptured 2-6 months later between ovulation and parturition, and individual reproductive status was then determined. Eighty-four females (65%) captured at the onset of vitellogenesis became vitellogenic, 45 did not. There was no difference in mean body length between reproductive and non-reproductive females. Initial body condition influenced reproductive outcome: we found a precise threshold in body condition necessary for the induction of vitellogenesis. Almost all females (88%) with a body condition greater than the observed threshold became vitellogenic, 12% did not, and no female with a body condition under the threshold became vitellogenic. Body reserves were estimated in the 129 living females using data gathered on 69 autopsied females. Females which became vitellogenic had large body reserves, but females which did not were not particularly emaciated (whilst postparturiant females had few body reserves remaining). This precise condition threshold for breeding is discussed in terms of the reproductive ecology of this species.