Review
Facultative placentotrophy: half-way house or strategic solution?1

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Abstract

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 ≤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.

Introduction

Considerable variation exists in the structural complexity of squamate placental systems (Stewart and Blackburn, 1988, Stewart, 1992, Blackburn, 1993, Stewart and Thompson, 1994, Stewart and Thompson, 1996). It is also apparent that there is an equally wide range in functional capacity of the placentae and that this contributes to a continuum of nutritional modes in lizards and snakes (Blackburn, 1994). This continuum ranges from the provision of water and respiratory gases only to a degree of obligate placentotrophy comparable to that found in therian mammals (Blackburn et al., 1984, Guillette, 1993).

Development based on a predominantly placental supply of nutrients appears so far to be restricted to the genus Mabuya (Blackburn et al., 1984), although the yolk supply is also very reduced in Pseudemoia pagenstecheri (Thompson and Stewart, 1994, Thompson et al., 1999a) and P. entrecasteauxii (Stewart and Thompson, 1993). In these species placentotrophy is obligate and successful embryonic development requires placental transfer of both organic and inorganic nutrients. In general, however, yolk remains the primary source of nutrients for the developing embryos of squamate reptiles. In at least some of these lecithotrophic species a proportion of the requirement for inorganic ions involves obligate placental transfer, but it is not clear if this is also true of organic compounds (Thompson et al., 1999a, Thompson et al., 1999c). What is clear, however, is that yolk nutrition can often be supplemented by placental transfer of both inorganic and organic chemicals (Stewart, 1989, Stewart and Thompson, 1993, Thompson et al., 1999a, Thompson et al., 1999b, Thompson et al., 1999c).

Supplementary transfer of nutrients in excess of the minimum requirements for successful development has been termed facultative placentotrophy (Stewart, 1989). Facultative placentotrophy has been demonstrated in a number of species by comparing the chemical composition of egg and neonates (Thompson et al., 1999a, Thompson et al., 1999b, Thompson et al., 1999c) but its physiological significance is unclear. We argue here that coupling facultative placentotrophy with lecithotrophy does not necessarily represent a transitional stage on the way to a complete dependence on placental nutrition. Our data suggest that it has adaptive value in its own right, through the provision of increased flexibility in nutrient delivery that allows females to enhance offspring fitness when circumstances are favorable.

Understanding the significance of facultative placentotrophy as a uniquely squamate adaptation among terrestrial amniotes requires experimental evidence of how, and in what circumstances, this nutritional mode occurs; such evidence is not available. In this paper we review a series of four experiments in which we have tried to gain insight into the role of facultative placentotrophy in the Australian skink, Niveoscincus metallicus. Individually, these experiments will be reported in greater detail elsewhere; our purpose here is to consider how, collectively, they may contribute to a greater understanding of the selective importance of facultative placentotrophy.

In order to do this we begin by summarizing the characteristics of the reproductive cycle of Niveoscincus metallicus, including the evidence for facultative placentotrophy, that make this species an appropriate test species. We then consider, from a theoretical perspective, how facultative placentotrophy might enhance reproductive success in this species. Since our experiments share common procedures for housing females during gestation and for assessing neonate fitness we describe these briefly, before presenting summary data for the four experiments that constitute this study.

Niveoscincus metallicus is a small lygosomine skink (2–4 g; snout-vent length (svl) 46–65 mm) that is widespread and locally extremely abundant on the island of Tasmania; it also occurs on the southeastern corner of mainland Australia. It is an annual breeder and, at least in lowland habitats, all females normally breed each year, producing 1–6 live young in mid-summer (Jones and Swain, 1996). Key features of the reproductive cycle are identified in Table 1. Experimentally, we have taken advantage of the high correlation between the number of follicles recruited and the size of the subsequent clutch (Jones and Swain, 1996), the large temporal displacement between when most vitellogenesis occurs and gestation, the relatively long gestation period, female sperm storage over winter, and the capacity to defer parturition if conditions are unsuitable.

Obligate placentotrophy involving the transfer of inorganic ions (Na+ and K+) has been demonstrated in this species (Thompson et al., 1999c). There is also strong circumstantial evidence for organic transfer (Jones et al., 1998, Thompson et al., 1999c), though whether any such transfer is necessary for successful reproduction has not been established. The capacity for amino acid transfer (using 3H-leucine) correlates with both the stage of embryonic development and the structural integrity of the placental membranes (Swain and Jones, 1997). Transfer of 3H-leucine and incorporation into embryonic protein is greatest between Stages 35 and 40, coinciding with the greatest elaboration of the placental membranes. Transfer was low before Stage 35, when the chorioallantoic membranes are relatively immature (Stewart and Thompson, 1994), and in the period after development is completed at Stage 40; this latter period normally lasts for about 3 weeks, during which time the yolk is finally consumed and both yolk and chorioallantoic placentae degenerate (Stewart and Thompson, 1994). From this time until birth, embryos must therefore survive on their own reserves, while they increase in mass from around 150 mg (minimum survival mass) to around 210 mg (average mass at birth).

Facultative placentotrophy may be easy to define, but it is difficult to demonstrate unambiguously. To date, the most convincing evidence (Stewart, 1989, Thompson et al., 1999a, Thompson et al., 1999b, Thompson et al., 1999c) is the demonstration that larger females give birth to larger offspring, but do not ovulate larger eggs. Niveoscincus metallicus meets this criterion; for example, neonates from large mothers may be 50% heavier than those from smaller mothers following gestation in benign laboratory conditions, even though the size of ovulated follicles does not correlate with maternal size (P=0.56) (Fig. 1). In accepting this criterion for the identification of facultative placentotrophy, it should be noted that, while the quantity of yolk does not depend on maternal size, variation in yolk quality (i.e. compositional variation) within or between females has received little attention.

Clutch size in this species is determined at the time of follicular recruitment; there is very little loss of potential offspring by atresia, embryo resorption, or abortion, yet recruitment commences almost 12 months before parturition (Jones and Swain, 1996). The Tasmanian climate ranges from cool to cold temperate, according to location (Rawlinson, 1974) and, due to the island's position in the ‘Roaring Forties’, is extremely changeable, on both diel and seasonal timescales. Niveoscincus metallicus occurs in all terrestrial habitats, except those in the alpine zone. Making a firm reproductive commitment when the future is so uncertain must involve risks, and we suggest that facultative placentotrophy provides a mechanism whereby N. metallicus may offset these risks. In seasons when conditions for gestation are average or poor, facultative placentotrophy may ensure successful reproduction by providing an alternative to clutch reduction; this ‘guarantee’ is likely to be particularly important in the period immediately before parturition, when birth may be deferred for several weeks. In better-than-average gestation conditions facultative placentotrophy may provide supplementary nutrition as a ‘bonus’ to the developing young.

Facultative placentotrophy might therefore influence offspring fitness in N. metallicus in a number of ways, as summarized in Table 2. Females are assumed to provide their eggs with optimum (good) yolk supplies in autumn if conditions during vitellogenesis are good (options A, B). If conditions are also good during spring (option A) then facultative placentotrophy can presumably supplement embryonic nutrition and enhance neonate condition at birth. Section 3, Section 4 and Section 5 examine neonate fitness in idealized reproductive circumstances. If, however, the mother experiences conditions that restrict her activity during gestation, leading to reduced basking opportunities and reduced food intake, her capacity to supplement nutrition during development will be minimal (option B; Section 4). If conditions are adverse during vitellogenesis, two options are possible for the mother (options C, D). Niveoscincus metallicus rarely achieve their maximum clutch potential (Jones and Swain, 1996), so the more likely scenario is that she will provision fewer eggs but provision each of these at an optimum level (option C), producing circumstances for facultative placentotrophy comparable to option A (Section 4). There may, however, be a minimum threshold of yolk provisioning (either in quality or quantity), in which case relatively poorly yolked eggs may be produced (option D); in these circumstances facultative placentotrophy may be essential if viable young are to be produced. Section 6 describes a preliminary investigation of this possibility using a novel approach to yolk reduction.

There is also the possibility that both vitellogenesis and gestation occur in adverse conditions (option E); the options for yolk supply may be as proposed for either option C or D but, in either event, the potential for facultative placentotrophy will be severely curtailed. The possibilities inherent in option E have not been investigated.

The contribution of facultative placentotrophy to embryonic development is not necessarily directed towards additional body mass. Indeed, in ‘ideal’ conditions, when minimum yolk is required as a substrate for embryonic maintenance metabolism, the yolk available for tissue growth may be quite sufficient to produce neonates in optimum physical condition — presumably this is what happens in species, including oviparous species, where facultative placentotrophy does not occur. Supplementation may instead be directed towards maximizing embryonic energy reserves (abdominal fat bodies in this species); these may serve an important role in maintaining embryonic fitness in the final gestational period, especially when a period of poor weather in summer results in birth being deferred. The significance of embryonic fat reserves in these circumstances is examined in Section 5.

Section snippets

Shared procedures

Except where otherwise stated, all animals for our experiments were maintained under common conditions. Niveoscincus metallicus females are non-aggressive and non-territorial, so we keep them in groups of 4 in small plastic containers (30×20×10 cm), each of which is supplied with bedding, a cool shelter, water ad libitum and an upturned terracotta bowl that serves as an additional (warm) retreat and basking site. Vitamin D plus a calcium supplement are added to the water. The species is a

Would young benefit from reduction in clutch size?

Females may have a finite capacity to supplement embryonic resources through facultative placentotrophy; presumably there are physiological limits to how much material can be transferred and how much energy can be directed towards this activity, and there is a limited ‘window of opportunity’ during development when transferal can occur (Swain and Jones, 1997). If the number of young is reduced, do the remaining young receive increased supplementation? We tested this possibility by surgically

Can facultative placentotrophy compensate for poor conditions during gestation?

As a result of recent interest in maternal effects in squamates, numerous phenotypic characteristics of neonates have been shown to be dependent on the thermal environment experienced prior to birth or hatching (e.g. Beuchat, 1988, Van Damme et al., 1992, Shine and Harlow, 1993, James and Whitford, 1994, Shine, 1993, Elphick and Shine, 1998). In contrast to endotherms, the ability of a viviparous lizard to maintain the environment in which her embryos develop is largely dependent on external

Do embryos utilize their own fat reserves when birth is delayed?

Section 4 led us to propose that facultative placentotrophy facilitates delayed parturition indirectly, by maximizing the establishment of embryonic energy reserves earlier in development. Support for this reasoning requires the demonstration that embryos do, indeed, call upon their own fat body reserves to a substantial extent when birth is deferred.

Within populations of N. metallicus, reproductive events tend to be closely synchronized. We took advantage of this by collecting approximately 90

Can facultative placentotrophy compensate for poor conditions during vitellogenesis?

One of the possibilities expressed in Table 2 is that facultative placentotrophy might provide a mechanism for making up deficits in yolk supply brought about by unfavorable conditions during vitellogenesis. We do not regard this as a likely possibility in N. metallicus. Since females of this species determine their clutch size at the time of follicular recruitment (Jones and Swain, 1996), it seems more probable that clutch size is determined by distributing the available resources for

Conclusion

Our experiments confirm that facultative placentotrophy does occur in N. metallicus. Since larger females meet Stewart's (Stewart, 1989) criteria for facultative placentotrophy, a large component of any maternal supplementation is presumably used to increase embryonic body bulk during development. However, our data strongly suggest that a further role for facultative placentotrophy, at least in N. metallicus, is to maximize embryonic fat stores. Fig. 3 indicates that large neonates have

Acknowledgements

Some of this work was carried out with financial support provided by the Australian Research Council small grants scheme, for which we are grateful. The work was authorized by the University of Tasmania Animal Ethics Committee under permit numbers 94072 and 97036.

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