Roy Swain

Maternal basking behaviour determines offspring sex in a viviparous reptile.

Two primary dichotomies within vertebrate life histories involve reproductive mode (oviparity versus viviparity) and sex determination (genotypic sex determination versus environmental sex determination). Although reptiles show multiple evolutionary transitions in both parameters, the co–occurrence of viviparity and environmental–dependent sex determination have heretofore been regarded as incompatible. Our studies on the viviparous lizard Niveoscincus ocellatus show that the extent of basking by a female influences the sex of her offspring. Critically, our data reveal this effect both in the field (via correlations between date of birth and litter sex ratio) and in a laboratory experiment (females with reduced basking opportunities produced more male offspring). Changes in thermoregulatory behaviour thus allow pregnant female lizards to modify the sex of their offspring.

MATERNAL-FETAL TRANSFER OF 3H-LABELLED LEUCINE IN THE VIVIPAROUS LIZARD NIVEOSCINCUS METALLICUS (SCINCIDAE: LYGOSOMINAE)

The entry of radio-labelled leucine into maternal and embryonic compartments was studied in the viviparous lizard, Niveoscincus metallicus , following its injection into gravid females. The label appeared rapidly in the maternal bloodstream and liver, where much of it was incorporated into hepatic peptides and proteins. Uptake into amniotic fluid, yolk and yolk sac membranes, and embryos was also rapid and, depending on the stage of development of the embryo, between 21 and 44% of the label that entered the embryo was incorporated into proteinaceous material 2 b after the mother was injected. Transfer into the embryo was significantly associated with embryonic stage of development. It was highest in embryos between Stages 35 and 40 when growth and development are most rapid and structural complexity of the placentae is at its peak. It was least in embryos younger than Stage 35, when placental development is rudimentary, and in late Stage 40 embryos that had utilized their yolk and were close to birth weight. We conclude that there is strong evidence for organic matrotrophy in N. metallicus and suggest that it provides a mechanism for supplementing yolk reserves during development in an unpredictable climate.

Geographic Variation in Age and Size at Maturity in a Small Australian Viviparous Skink

Abstract Age and size at maturity are pivotal life-history traits through their effects on other key traits, such as annual and lifetime fecundity. We used skeletochronology to investigate the relationships among size (snout–vent length), age, and maturity in two populations of a small viviparous skink, Niveoscincus ocellatus, from Tasmania, Australia. The species occupies a wide geographic and climatic range within the temperate zone, and we chose populations from the climatic extremes of this range. Growth in N. ocellatus is rapid early in life but slows considerably after maturity in both sexes. Within sites, we found no difference in growth patterns or length at maturity between the sexes. However, there were large differences between sites. At our “warm” site, lizards were mature at three years of age at a relatively small size. Lizards from the “cold” site typically delayed maturity until their fourth year (although some males were mature at the end of their third year); as a result, they were significantly larger at maturity and thereafter remained larger for any age than did warm-site lizards. These patterns are consistent with predictions from models of the proximate influence of the thermal environment on growth and maturity patterns in squamate reptiles. Lizards from the cold site are born later in the season and have a shorter activity season prior to obligatory winter hibernation, and conditions for growth are less favorable in any particular month than at the warm site. Because delaying maturity is costly to current fecundity, we suggest that in N. ocellatus lifetime fecundity is enhanced at the cold site by additional growth and gains in future fecundity through the relationship between body length and reproductive output.

Annual reproductive cycle and annual cycles of reproductive hormones in plasma of female Niveoscincus metallicus (Scincidae) from Tasmania

Niveoscincus metallicus is a small viviparous skink common in Tasmania. We describe the annual reproductive cycle of female N. metallicus and relate this to changes in plasma levels of progesterone and estradiol. Vitellogenesis begins in autumn (March), with first matings in April, prior to entering winter torpor. Ovulation occurs in mid-September about two weeks after spring emergence. Size adjusted atresia of vitellogenic follicles was 8% in the population studied. No loss of embryos in utero was observed and young are born in January. Plasma estradiol levels are significantly elevated during the preovulatory phase. Progesterone concentrations are low through most of the year but rise during gestation and are highest during the second trimester, declining well before parturition.

Maternal effects associated with gestation conditions in a viviparous lizard, Niveoscincus metallicus

Viviparous squamates offer opportunities for exploring the importance of past maternal resources (yolk) and current resources (placentotrophy) to support embryonic growth during gestation, and to optimize offspring fitness. Both thermal and nutritional environment of the mother during gestation may be expected to be important in determining offspring fitness. Using a two-way factorial design, we have investigated possible interactions between food intake and thermal environment during gestation in the viviparous skink Niveoscincus metallicus . Among the females given restricted basking opportunities, fewer females gave birth, there was a significant increase in gestation length, and relative clutch mass was reduced due to smaller neonatal size; none of these parameters were influenced by nutritional status. Neonates from mothers given restricted basking opportunities were lighter, had shorter snout-vent lengths (SVL), and smaller fat bodies than neonates from mothers given optimal basking opportunities; their postnatal growth rate (over eight weeks) was also significantly lower and they showed a reduced incidence of basking behavior. There were interaction effects between thermal regime and food supply for neonate SVL and neonatal fat body weight. Sprint speed within 24 hours of birth was significantly increased in neonates from mothers given restricted thermal opportunities; however, for weeks 1-8 postnatally, there were no differences in sprint speed in offspring from any of the treatments. These results suggest that, contrary to our initial hypothesis, females maintained in nutritionally favorable conditions are unable to compensate for the gestational effects of a thermally poor environment. We now suggest that in Niveoscincus metallicus facultative placentotrophy may allow mothers to improve offspring fitness by increasing neonatal fat body size.

Facultative placentotrophy: half-way house or strategic solution?

While yolk is generally the primary source of embryo nutrients in squamates, numerous species supplement this with facultative placentotrophy. We argue that facultative placentotrophy should have selective importance relevant to offspring fitness. In the skink Niveoscincus metallicus, the size of ovulated eggs is unrelated to maternal size but large females produce offspring that are larger than is necessary for survival, providing evidence for facultative placentotrophy. We discuss the circumstances in which facultative placentotrophy might be used to supplement the nutritional support provided by yolk and obligate placentotrophy in this species, and present summary data from experiments designed to investigate these circumstances. Clutch reduction by oviduct removal had no effect on neonate mass or snout-vent length, indicating that the number of embryos does not influence allocation of maternal resources once gestation has commenced. Manipulation of maternal basking opportunity in combination with food intake during pregnancy suggested that an important role of facultative placentotrophy is the optimization of embryonic fat reserves. This hypothesis was supported by the observation that larger neonates have larger abdominal fat bodies. These reserves presumably facilitate survival in the relatively short pre-hibernatory period available to newborn animals. Our data indicate that they also play a vital role in maintaining pre-natal condition if birth is delayed by adverse weather, a common circumstance in this species. In such circumstances the yolk has been used up and the placental membranes have degenerated. Experimental induction of premature ovulation of eggs with reduced yolk, achieved by injecting females with FSH, was followed by fertilization using stored sperm. Gestation length was greatly reduced and the resulting neonates were all < or =75% normal birth mass, with two of the six births being stillborn. Thus facultative placentotrophy does not appear to be a means of compensating for a poor yolk supply. We suggest that facultative placentotrophy in N. metallicus is not a transitional stage en route to greater reliance on obligate placentotrophy, but a uniquely squamate adaptation that provides flexibility in embryonic nutrition, and optimizes offspring fitness in an unpredictable temperate climate.

Changes in Reproductive Investment following Caudal Autotomy in Viviparous Skinks (Niveoscincus metallicus): Lipid Depletion or Energetic Diversion?

Abstract The effect of caudal autotomy on reproductive investment in females of a viviparous skink, Niveoscincus metallicus, was investigated to examine the relative importance of lipid depletion and energetic diversion to this activity. Although abdominal fat bodies are present, this species stores most of its energetic reserves in the tail. Since caudal fat is preferentially aggregated toward the base of the tail, autotomy and lipid depletion may be mutually exclusive events. Reproductive consequences following tail loss associated with significant loss of caudal fat were compared with those following autotomy involving no fat loss in two groups of females: females that had lost their tail during their most recent vitellogenic period; and females in which tail loss had occurred in a previous reproductive season. Caudal autotomy during vitellogenesis resulted in a significant reduction in litter size, irrespective of the position of tail loss, suggesting that smaller litters were a consequence of the diversion of energetic resources from reproduction to tail regeneration, rather than the loss of fat reserves per se. However, offspring from mothers that experienced tail loss during vitellogenesis without associated loss of fat reserves were significantly larger in size (snout–vent length and mass) and had longer tails than those from any other group. We suggest that this was probably achieved through facultative placental transfer during gestation, although the possibility that more yolk was allocated to each egg cannot be discounted. Sprint speed and the size of abdominal fat reserves at birth and postnatal growth were not correlated with either recency of autotomy or the location of the tail break.

Effect of Tail Loss on Sprint Speed and Growth in Newborn Skinks, Niveoscincus metallicus

Abstract Most studies that examined effects of caudal autotomy on lizards focused on adults and largely neglected the potential for contrasting effects in newborns and juveniles. We examined the impact of tail autotomy on locomotor performance and growth in newborn Metallic Skinks, Niveoscincus metallicus. Two siblings were randomly selected from each of 12 litters, with one assigned to a control group (tail intact) and the other to an experimental group (tail removed). Removal of the tail at the base 24 h after birth resulted in a significant decrease in sprint speed 72 h after birth (approximately 50% reduction compared to speed within 24 h of birth). This impairment is substantially greater than that observed previously in adults of this species (35%). However, caudal autotomy at birth did not inhibit growth, measured as the increase in snout–vent length, during the first eight weeks of life. Despite maintaining growth rate, newborns were still able to regenerate at least one-third of their tail over the eight weeks of the study. We discuss how the absence of the tail, the presumed energetic cost of tail replacement, and the lack of caudal fat stores, may influence the ability of newborn N. metallicus to survive their first winter.

Feeding ecology of the Tasmanian spotted skink, Niveoscincus ocellatus (Squamata : Scincidae)

The feeding ecology of the spotted skink, Niveoscincus ocellatus, was examined over a 6-month period, from October to March, with additional data from one sample in midwinter. The investigation considered feeding activity, dietary composition and foraging strategy. Feeding activity,measured by stomach fullness, was unrelated to age, sex or reproductive status and showed little variation during the warmer months; in winter feeding was greatly reduced. N. ocellatus exhibits flexible foraging behaviour; a wide variety of terrestrial arthropods is taken opportunistically in accordance with a wide ranging foraging strategy. However, the consistent occurrence of cryptic and hidden prey indicates that active search foraging is also utilised. No evidence for ambush predation was found and, unlike many other small skinks, few arboreal or aerial prey are included in the diet, even though the habitat is rock scree and woodland where such prey abound. No evidence for any in a specific partitioning of diet based on kind or size of prey was obtained although a slight, but significant, correlation exists between maximum prey size and lizard size.

Delayed ovulation and parturition in a viviparous alpine lizard (Niveoscincus microlepidotus): morphological data and plasma steroid concentrations

The southern snow skink, Niveoscincus microlepidotus, exhibits an unusual biennial reproductive cycle with an extended gestation period of approximately 1 year. Morphological data were gathered on a monthly basis, providing a detailed picture of the reproductive cycle. Vitellogenesis begins in spring, immediately after parturition. Maximum follicular diameter is reached before the winter hibernation period and ovulation occurs the following spring. Embryos are fully developed and reach maximum size by early autumn. Yolk reserves are depleted before winter. Birth of between one and four young occurs the following spring. Plasma progesterone concentrations are low (2.7 +/- 0.9 ng mL(-1)) in post-partum females, begin to rise in autumn in vitellogenic females and peak (38.5 +/- 7.9 ng mL(-1)) in pre-ovulatory females after hibernation. Concentrations are high (15.4 +/- 5.9 ng mL(-1)) in early pregnancy and decline to basal levels before winter and well before birth in spring. Plasma oestradiol concentrations peak during vitellogenesis (1.0 +/- 0.3 ng mL(-1)) and decline to basal levels during pregnancy (0.2 +/- 0.03 ng mL(-1)). A second oestradiol peak occurs before parturition (0.7 +/- 0.2 ng mL(-1)). Thus, functional completion of vitellogenesis and gestation is achieved by autumn in successive years. The mechanisms that defer ovulation and parturition by a further six months are unknown.