Wei-Guo Du

Does body-volume constrain reproductive output in lizards?

The numbers and sizes of eggs produced by adult females ultimately determine the viability of populations, as well as the evolutionary fitness of the females themselves. Despite an enormous amount of literature on the adaptive significance of fecundity variation within and among populations, simpler questions—such as the proximate mechanisms by which a female determines her clutch size—have attracted less attention. Our surgical manipulations show that the amount of space available to hold eggs within a females abdomen influences her total reproductive allocation, enabling her to flexibly modify her reproductive output as she grows larger.

Determinants of incubation period: do reptilian embryos hatch after a fixed total number of heart beats?

SUMMARY The eggs of birds typically hatch after a fixed (but lineage-specific) cumulative number of heart beats since the initiation of incubation. Is the same true for non-avian reptiles, despite wide intraspecific variation in incubation period generated by variable nest temperatures? Non-invasive monitoring of embryo heart beat rates in one turtle species (Pelodiscus sinensis) and two lizards (Bassiana duperreyi and Takydromus septentrionalis) show that the total number of heart beats during embryogenesis is relatively constant over a wide range of warm incubation conditions. However, incubation at low temperatures increases the total number of heart beats required to complete embryogenesis, because the embryo spends much of its time at temperatures that require maintenance functions but that do not allow embryonic growth or differentiation. Thus, cool-incubated embryos allocate additional metabolic effort to maintenance costs. Under warm conditions, total number of heart beats thus predicts incubation period in non-avian reptiles as well as in birds (the total number of heart beats are also similar); however, under the colder nest conditions often experienced by non-avian reptiles, maintenance costs add significantly to total embryonic metabolic expenditure.

Behavioral thermoregulation by turtle embryos

Mobile ectothermic animals can control their body temperatures by selecting specific thermal conditions in the environment, but embryos—trapped within an immobile egg and lacking locomotor structures—have been assumed to lack that ability. Falsifying that assumption, our experimental studies show that even early stage turtle embryos move within the egg to exploit small-scale spatial thermal heterogeneity. Behavioral thermoregulation is not restricted to posthatching life and instead may be an important tactic in every life-history stage.

Natural History Note The Physiological Basis of Geographic Variation in Rates of Embryonic Development within a Widespread Lizard Species

The duration of embryonic development (e.g., egg incubation period) is a critical life‐history variable because it affects both the amount of time that an embryo is exposed to conditions within the nest and the seasonal timing of hatching. Variation in incubation periods among oviparous reptiles might result from variation in either the amount of embryogenesis completed before laying or the subsequent developmental rates of embryos. Selection on incubation duration could change either of those traits. We examined embryonic development of fence lizards (Sceloporus undulatus) from three populations (Indiana, Mississippi, and Florida) that occur at different latitudes and therefore experience different temperatures and season lengths. These data reveal countergradient variation: at identical temperatures in the laboratory, incubation periods were shorter for lizards from cooler areas. This variation was not related to stage at oviposition; eggs of all populations were laid at similar developmental stages. Instead, embryonic development proceeded more rapidly in cooler‐climate populations, compensating for the delayed development caused by lower incubation temperatures in the field. The accelerated development appears to occur via an increase in heart mass (and, thus, stroke volume) in one population and an increase in heart rate in the other. Hence, superficially similar adaptations of embryonic developmental rate to local conditions may be generated by dissimilar proximate mechanisms.

The behavioural and physiological strategies of bird and reptile embryos in response to unpredictable variation in nest temperature

Temperature profoundly affects the rate and trajectory of embryonic development, and thermal extremes can be fatal. In viviparous species, maternal behaviour and physiology can buffer the embryo from thermal fluctuations; but in oviparous animals (like most reptiles and all birds), an embryo is likely to encounter unpredictable periods when incubation temperatures are unfavourable. Thus, we might expect natural selection to have favoured traits that enable embryos to maintain development despite those fluctuations. Our review of recent research identifies three main routes that embryos use in this way. Extreme temperatures (i) can be avoided (e.g. by accelerating hatching, by moving within the egg, by cooling the egg by enhanced rates of evaporation, or by hysteresis in rates of heating versus cooling); (ii) can be tolerated (e.g. by entering diapause, by producing heat‐shock proteins, or by changing oxygen use); or (iii) the embryo can adjust its physiology and/or developmental trajectory in ways that reduce the fitness penalties of unfavourable thermal conditions (e.g. by acclimating, by exploiting brief windows of favourable conditions, or by producing the hatchling phenotype best suited to those incubation conditions). Embryos are not simply passive victims of ambient conditions. Like free‐living stages of the life cycle, embryos exhibit behavioural and physiological plasticity that enables them to deal with unpredictable abiotic challenges.

Thermal Acclimation of Heart Rates in Reptilian Embryos

In many reptiles, the thermal regimes experienced by eggs in natural nests vary as a function of ambient weather and location, and this variation has important impacts on patterns of embryonic development. Recent advances in non-invasive measurement of embryonic heart rates allow us to answer a long-standing puzzle in reptilian developmental biology: Do the metabolic and developmental rates of embryos acclimate to local incubation regimes, as occurs for metabolic acclimation by post-hatching reptiles? Based on a strong correlation between embryonic heart rate and oxygen consumption, we used heart rates as a measure of metabolic rate. We demonstrate acclimation of heart rates relative to temperature in embryos of one turtle, one snake and one lizard species that oviposit in relatively deep nests, but found no acclimation in another lizard species that uses shallow (and hence, highly thermally variable) nests. Embryonic thermal acclimation thus is widespread, but not ubiquitous, within reptiles.

Chemical cues from both dangerous and nondangerous snakes elicit antipredator behaviours from a nocturnal lizard

Many prey species use chemical cues to detect predators. According to the threat sensitivity hypothesis, prey should match the intensity of their antipredator behaviour to the degree of threat posed by the predator. Several species of lizards display antipredator behaviours in the presence of snake chemical cues, but how species specific are these responses? In Australia, most snake species eat lizards, and are therefore potentially dangerous. Hence, we predicted that lizards should display generalized rather than species-specific antipredator behaviours. To test this prediction, we quantified the behavioural responses of velvet geckos, Oedura lesueurii, to chemical cues from five species of elapid snakes that are syntopic with velvet geckos but differ in their degree of danger. These five snake species included two nocturnal ambush foragers that eat geckos (broad-headed snake Hoplocephalus bungaroides, and death adder, Acanthophis antarcticus), two active foragers that eat skinks (but rarely eat geckos) and that differ in their activity times (nocturnal small-eyed snake, Cryptophis nigrescens, and diurnal whip snake, Demansia psammophis), and a nocturnal nonthreatening species that feeds entirely on blind snakes (bandy-bandy, Vermicella annulata). Geckos showed similar antisnake behaviours (tail waving, tail vibration), and a similar intensity of responses (reducing activity, freezing), to chemical cues from all five snake species, even though the snakes differed in their degree of danger and foraging modes. Our results suggest that velvet geckos display generalized antipredator responses to chemicals from elapid snakes, rather than responding in a graded fashion depending upon the degree of threat posed by a particular snake species.

Phenotypic Effects of Thermal Mean and Fluctuations on Embryonic Development and Hatchling Traits in a Lacertid Lizard, Takydromus septentrionalis

How fluctuating temperatures influence reptilian embryos and hatchlings has attracted increasing scientific attention, but is poorly known. We conducted an incubation experiment with a factorial design of two mean temperatures (24 vs. 28 degrees C) and three diel thermal fluctuations (0, +/-3, +/-6 degrees C) to determine the effects of diel thermal fluctuations and mean temperature on incubation duration and hatchling phenotypes. Both diel thermal fluctuations and mean temperature significantly affected incubation duration, but not hatching success. Incubation duration increased with increasing temperature fluctuations at a mean temperature of 24 degrees C, but not at a mean temperature of 28 degrees C. The significant interaction between diel thermal fluctuations and mean temperature on hatchling morphology indicated that the effect of thermal fluctuations depended on the mean temperature. Hatchling mass differed significantly between 24+/-6 and 28+/-6 degrees C, but not between the two constant temperatures or the temperatures with +/-3 degrees C fluctuations. At a mean temperature of 24 degrees C, the effect of thermal fluctuations on hatchling size was marginally significant, with relatively large hatchlings at the constant temperature; at a mean temperature of 28 degrees C, thermal fluctuations had no impact on hatchling size. The locomotor performances were significantly affected by mean temperature rather than diel thermal fluctuations. Therefore, diel thermal fluctuations around a given mean temperature do not affect hatchling phenotypes in a relatively large magnitude, but the influence of diel thermal fluctuations may differ with changing mean temperatures.

Do operational sex ratios influence sex allocation in viviparous lizards with temperature-dependent sex determination?

Under certain environmental situations, selection may favour the ability of females to adjust the sex ratio of their offspring. Two recent studies have suggested that viviparous scincid lizards can modify the sex ratio of the offspring they produce in response to the operational sex ratio (OSR). Both of the species in question belong to genera that have also recently been shown to exhibit temperature‐dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field‐based experiments, and conduct the first field‐based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring.

The influence of hydric environments during egg incubation on embryonic heart rates and offspring phenotypes in a scincid lizard (Lampropholis guichenoti)

Extensive evidence shows that incubation conditions can affect phenotypic traits of hatchling reptiles, but the relative importance of thermal versus hydric factors, and the proximate mechanisms by which such factors influence hatchling phenotypes, remain unclear for most species. We incubated eggs of an Australian scincid lizard, Lampropholis guichenoti, at four different moisture contents ranging from -500 to 0 kPa. Drier substrates reduced water uptake of eggs and resulted in smaller hatchlings, but other phenotypic traits (incubation periods, hatchling sex, body proportions, running speeds, growth rates post-hatching) were not affected by the hydric environment during incubation. Contrary to our prediction, lower water uptake during incubation (and hence, presumably, more viscous blood) did not affect embryonic heart rates. Thus, as in many other squamate species, hatchling phenotypes and embryonic developmental rates of L. guichenoti are less sensitive to hydric conditions in the nest than to thermal regimes.