Eulamprus Tympanum)

Ecology, 79(3), 1998, pp. 1073±1083 q 1998 by the Ecological Society of America REPRODUCTIVE ENERGY ALLOCATION AND LONG-TERM ENERGY STORES IN A VIVIPAROUS LIZARD (EULAMPRUS TYMPANUM) PAUL DOUGHTY1 AND RICHARD SHINE School of Biological Sciences, A08, University of Sydney, New South Wales 2006, Australia Abstract. When animals reproduce, does energy for the brood come from stored reserves (from food eaten months or years before), or from food eaten during the current reproductive season? Variation in the duration of energy storage prior to reproduction is an important, but little-studied, axis of life history variation. We experimentally manipulated the availability of resources to females of a long-lived viviparous lizard (Eulamprus tympanum, Scincidae) in the ®rst year of a two-year study to assess the relative importance of current food intake vs. stored reserves as sources of energy for breeding. Females given greater access to high temperatures (and hence, to resources) in the laboratory amassed larger caudal energy stores than did females with lesser opportunities. Energy intake during gestation slightly in¯uenced offspring size, but the magnitude of energy stores prior to ovulation had a more dramatic effect: females with larger caudal energy stores produced much larger litters in the following year. Growth rates of females were unaffected by basking treatments or by reproduction in either year, but females that reproduced in the second year showed a large concomitant decrease in caudal energy stores compared to females that did not reproduce, indicating a large energetic cost of reproduction. Hence, reproductive output within this species can be in¯uenced by resource availability over 12 months prior to reproduction, and simple comparisons of reproductive output with current resource availability may fail to detect the ways in which phenotypically plastic life history traits are in¯uenced by environmental features. In addition to an appropriate temporal framework, models of resource allocation should also incorporate the possible roles of physiological and morphological constraints (e.g., maternal inability, in some species, to modify post- ovulation reproductive expenditure) and trade-offs with other life history currencies (e.g., decrements in maternal survival due to high relative clutch masses). The time lag between resource acquisition and expenditure may have signi®cant consequences for a population's demographic response to shifts in resource availability or predation pressure (via tail au- totomy). Finally, this study illustrates the way in which thermal aspects of the environment can in¯uence life history phenotypes in ectothermic vertebrates with long-term energy stores. Key words: energy allocation; Eulamprus tympanum; life history; lizard; reproduction; Scincidae; storage; time lags; trade-offs. INTRODUCTION ered a considerable time prior to their expenditure, because of the scarcity or ephemeral nature of the re- The relative allocation of an organism's available source in question (e.g., Hahn and Tinkle 1965, Fraser resources among the competing demands of mainte- 1980, Reznick and Yang 1993, Chastel et al. 1995). nance, growth, and reproduction has been a central Thus, the magnitude and duration of the storage of theme of research into life history ``strategies'' ever resources, and their patterns of subsequent use, rep- since R. A. Fisher ®rst raised the question in 1930. resent important, but little-explored, axes of interspe- Although most work in this ®eld has focused on energy ci®c and intraspeci®c variation. acquisition and expenditure, there is a growing rec- From a life history perspective, reliance on energy ognition that one important component of Fisher's orig- storage ultimately concerns the bene®ts and costs of inal formulation has been largely neglected. This is the different schedules of energy acquisition and expen- issue of energy storage (e.g., Reznick and Braun 1987, diture (e.g., Fisher 1930, Hahn and Tinkle 1965, Rez- Hom 1988, Dunham et al. 1989, Perrin and Sibly 1993, nick and Braun 1987, Dunham et al. 1989, Perrin and Bernardo 1994, Rollo 1995, JoÈnsson 1997). There are Sibly 1993, Reznick and Yang 1993, Chastel et al. many circumstances in which resources must be gath- 1995). Energy storage can be advantageous because it enables an organism to decouple the acquisition of en- Manuscript received 2 August 1996; revised 23 April 1997; ergy from its expenditure on functions such as growth accepted 28 April 1997. 1 Present address: Department of Zoology, University of or reproduction. For example, if resources are plentiful Western Australia, Nedlands, Western Australia 6907, Aus- early in the year and conditions are favorable for off- tralia. spring survival later in the year, then energy storage 1073 1074 PAUL DOUGHTY AND RICHARD SHINE Ecology, Vol. 79, No. 3 can allow an organism to ``save'' and ``spend'' energy the role of energy storage in reproduction. These me- (in economic terms) at different times, such that pa- dium-sized (;85 mm snout±vent length, 10 g body rental ®tness is maximized. Additionally, if the re- mass) diurnal scincid lizards are long-lived (.12 years sources necessary for a reproductive bout must be gath- in the wild, based on skeletochronology data; Tilley ered over a long period of time, then storage can pro- 1984; see also Blomberg 1994), and each year a large vide a means by which energy can be amassed and proportion of adult females does not reproduce spent in a single, large brood. This strategy, whereby (Schwarzkopf 1991, 1993, Rohr 1997). Eulamprus are reproduction is delayed (i.e., opportunities for repro- viviparous, but placental transfer of nutrients is be- duction are skipped) until the female has suf®cient en- lieved to be minimal; reproductive energy is allocated ergy to ®ll up her body cavity with embryos, may en- mostly at ovulation (Thompson 1981). Because the off- hance maternal ®tness if reproduction imposes high spring are nutritionally independent from birth, a fe- ``costs'' (in energy or risk) that are independent of the male's total energetic investment in her brood is con- level of fecundity (Bull and Shine 1979). In some cases, tained within the litter at parturition. the duration of energy storage may be very long. Less- The phylogenetic lineage of skinks that includes E. than-annual reproductive frequencies are common in tympanum is unusual in lacking abdominal fat bodies, long-lived species of lizards (e.g., Van Wyk 1991, so that the primary energy store is the base of the tail Schwarzkopf 1993, Cree and Guillette 1995), snakes (Greer 1986, 1989, Doughty 1996a, Doughty and Shine (e.g., Saint-Girons 1982, Seigel and Fitch 1985, Shine 1997, Rohr 1997; see also Taylor 1986, Xiang et al. 1986, Naulleau and Bonnet 1996), turtles (e.g., Gib- 1994). In the current study, we chose to focus on caudal bons and Semlitsch 1982, Limpus et al. 1984), and energy stores because of the wide variation in tail thick- salamanders (e.g., Maiorana 1977, Fraser 1980, Scott ness of adult females observed in the wild (from 6.5 and Fore 1995). mm to 11.0 mm; P. Doughty, unpublished data), and Ectothermic vertebrates thus provide some of the because of the negative correlation between reproduc- best examples of reproduction that is fuelled by energy tion and caudal energy stores in a closely-related spe- gathered over a long period prior to the time of ovu- cies that also lacks abdominal fat bodies (Taylor 1986; lation, rather than energy gathered during gestation see also Castilla and Bauwens 1990). Without invasive (e.g., Fraser 1980, Reznick 1983, Schultz et al. 1991, or lethal procedures, we assessed energy stores by mea- Naulleau and Bonnet 1996). However, work on small, suring the width of the tailbase, which is correlated short-lived species has provided both correlational with the amount of lipids stored in the tail (Doughty (e.g., Derickson 1976a, Ballinger 1977, Jones et al. 1996a). 1987, Smith et al. 1995) and experimental (Guyer 1988, The montane environment occupied by E. tympanum Ford and Seigel 1989, Reznick and Yang 1993, James has a cool and variable climate, which strongly affects and Whitford 1994, Jokela and Mutikainen 1995) ev- the animals' opportunities to maintain high body tem- idence that prey availability can in¯uence reproductive peratures. Such environmental constraints have strong output within a single season. It appears that repro- effects on these lizards' rates of feeding, digestion, and, ductive output in such taxa can be modi®ed relatively for gravid females, rates of embryogenesis that deter- quickly in response to changes in energy availability. mine the duration of pregnancy (Schwarzkopf and Nonetheless, studies of short-lived species are poorly Shine 1991, 1992, Blomberg 1994, Doughty 1996a). suited to analyses of longer term effects of energy stor- Thus, by modifying basking opportunities in the lab- age on reproductive output. If we are to develop general oratory, we were able to manipulate females' rates of models of energy allocation in ectotherms, and es- feeding and energy assimilation. This population of E. pecially if we are to determine whether patterns of tympanum has been under study since 1987, and much energy allocation differ fundamentally between long- is known of its demography, behavior, and reproduction and short-lived species (Sauer and Slade 1987, Wei- (Schwarzkopf 1991, 1992, 1993, Schwarzkopf and merskirch 1992, Perrin and Sibly 1993, Schwarzkopf Shine 1991, 1992, Blomberg 1994, Doughty 1996a, 1993), then data on long-lived species (including or- Doughty and Shine 1997; see also Rohr 1997). ganisms that frequently skip opportunities for reproduction) are essential. In this paper, we describe an Experimental design experimental study on such an organism, to explore the In the ®rst year of the study, we manipulated basking role of energy storage in ectotherm reproduction, and opportunities of female water skinks during gestation speci®cally the degree to which reproduction is fuelled (that is, after litter size had been determined) to ex- by recently ingested energy vs.

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