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Making Eggs from Nectar: the Role of Life History and Dietary Carbon Turnover in Butterfly Reproductive Resource Allocation

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Making Eggs from Nectar: the Role of Life History and Dietary Carbon Turnover in Butterfly Reproductive Resource Allocation OIKOS 105: 279Á/291, 2004 Making eggs from nectar: the role of life history and dietary carbon turnover in butterfly reproductive resource allocation Diane M. O’Brien, Carol L. Boggs and Marilyn L. Fogel O’Brien, D. M., Boggs, C. L. and Fogel, M. L. 2004. Making eggs from nectar: the role of life history and dietary carbon turnover in butterfly reproductive resource allocation. Á/ Oikos 105: 279Á/291. The diets of many butterflies and moths change dramatically with development: from herbivory in the larvae to nectarivory in the adults. These diets are nutritionally distinct, and thus are likely to contribute differentially to egg manufacture. We examine the use of dietary resources in egg manufacture by four butterfly species with different patterns of oviposition and lifespan; three in the Nymphalidae (Euphydryas chalcedona, Speyeria mormonia and Heliconius charitonia), and one in the Pieridae (Colias eurytheme). Each species was fed two isotopically distinct adult diets based on sucrose, both of which differed from the larval hostplant in 13C content. Egg isotopic composition was analyzed to quantify the contribution of carbon from the larval and adult diets to egg manufacture. In all four species, egg 13C content increased to an asymptotic maximum with time, indicating that adult diet is an increasingly important source of egg carbon . The 13C increase closely resembled that of a nectar-feeding hawkmoth, and was well-described by a model of carbon flow proposed for that species. This similarity suggests that the turnover from larval to adult dietary support of egg manufacture is conserved among nectar-feeding Lepidoptera. Species varied widely in the maximum % egg carbon that derives from the adult diet, from 44% in E. chalcedona to nearly 80% in S. mormonia. These differences were related both to the extent of oocyte provisioning prior to adult emergence, and to egg composition. A species’ lifetime use of larval vs adult resources in egg manufacture reflected both the carbon turnover of the eggs and the timing of oviposition. Thus, the extent to which dietary resources are important in egg manufacture in butterflies depends on development (egg provisioning in teneral adults), behavior (timing of oviposition) and nutritional physiology (nutrient synthesis and turnover). D. M. O’Brien and C. Boggs, Center for Conservation Biology, Dept of Biological Sciences, Stanford Univ., Stanford, CA 94305. Present address for DMO: Dept of Biological Sciences, Wellesley College, 106 Central St., Wellesley, MA 02481, USA ([email protected]). Á/ M. Fogel, Geophysical Laboratory, Carnegie Institution of Washington, 5251 Broad Branch Rd. NW, Washington DC 20015, USA. Assumptions about how organisms use nutritional as a currency for reproduction and survival, other resources are fundamental to predictions about life nutrients, such as nitrogen (Slansky and Feeny 1977, history and evolutionary ecology (Reznick 1985, Stearns Brodbeck et al. 1993), phosphorous (Elser et al. 1996, 1992, Rose and Bradley 1998). Nutrition is a key Markow et al. 1999), or essential carbon compounds determinant of reproduction (Wheeler 1996); therefore, (Douglas 1998, O’Brien et al. 2002) may pose greater reproductive strategies need to be considered in light of constraints upon reproduction and population growth. nutrient availability (Boggs 1992, de Jong and van The complexities of nutrient requirements, synthesis, Noordwijk 1992). Although energy is commonly used storage, conversion and metabolism are poorly under- Accepted 25 September 2003 Copyright # OIKOS 2004 ISSN 0030-1299 OIKOS 105:2 (2004) 279 stood, especially for free-living animals with mixed or enabled them to trace carbon use in eggs with high complex diets. There is a growing appreciation for the accuracy, and they proposed a descriptive carbon turn- physiological complexity of resource allocation (Rose over model to describe how egg nutrients were incorpo- and Bradley 1998, Rivero and Casas 1999, Zera and rated into eggs (O’Brien et al. 2000). Harshman 2001, Zhao and Zera 2002), in particular, for In this study, we apply a similar approach to hormonal controls of nutrient use (Sinervo and Svensson investigate the dietary sources of reproductive nutrients 1998, Zera et al. 1998). A similar focus on nutritional in four nectar-feeding butterfly species, three from the physiology will further help to strengthen the connec- family Nymphalidae and one from the family Pieridae. tions between diet and life history. The species selected exhibit a range of variation in Resource allocation in holometabolous insects is lifespan and age-specific fecundity, and differ in degree particularly interesting because diets and energetic needs of shared phylogenetic history. We investigate whether change between life stages, causing nutrient intake and the turnover pattern modeled in hawkmoth eggs is nutrient demand to be temporally separated (Boggs exhibited in other nectar-feeding Lepidoptera. If so, we 1981, 1986, Rivero et al. 2001). In these insects, evaluate whether the extent of adult diet use or the mechanisms for appropriately timed nutrient storage rapidity of larval to adult diet turnover vary according to and release are extremely important (Delobel et al. 1993, differences in life history. We predict that the reliance on Wheeler and Buck 1995, Snigirevskaya et al. 1997, adult dietary carbon in egg manufacture will be higher in Djawdan et al. 1998, Wheeler et al. 2000, Pan and Telfer those species whose reproductive effort takes place later 2001). In most butterflies and many moths, diets change in the adult lifespan. dramatically from herbivory in the larvae to nectarivory This study uses sucrose solution as an experimental in the adults. These diets are nutritionally distinct, and proxy for the adult nectar diet, as it elicts a strong thus are likely to contribute differently to physiological feeding response from butterflies (Romeis and Wa¨ckers demands. Nectar is rich in sugars but relatively depau- 2000) and is easy to acquire in different isotopic forms. perate in amino acids, fatty acids, and other nutritionally This proxy is a nutritional oversimplication, especially as important compounds (Baker and Baker 1983). The some butterflies have been shown to detect and slightly larval diet is the primary supply of protein, which is prefer nectars containing amino acids (Alm et al. 1990, stored for use during metamorphosis and oogenesis Rusterholz and Erhardt 1998, Mevi-Schutz and Erhardt (Wheeler et al. 2000, Pan and Telfer 2001). Butterfly 2002). We do not suggest that other dilute components researchers have long appreciated that both larval and of nectar could not play some nutritional role in adult diets are important to reproduction and are both oviposition. This study might slightly underestimate used in egg manufacture (Norris 1934, Dunlap-Pianka et the importance of the adult diet in species that capitalize on nectar amino acids. However, as the vast majority of al. 1977, Hill 1989, Hill and Pierce 1989, Alm et al. 1990, carbon provided by the adult diet is in the form of sugar Boggs and Ross 1993, Boggs 1997a). Because their life (Baker and Baker 1983), sugar is a reasonable proxy histories vary, the Lepidoptera have also provided a given our carbon isotope mass-balance approach. model system for comparing reproductive output among species with varying degrees and types of adult foraging (Boggs 1986, 1990, 1992, 1997b, 2003). We use natural variation in 13C to identify egg carbon Methods deriving from the larval and adult diets in butterflies with nectivorous adults, but differing lifespans and age- Study organisms specific fecundities. 13C content differs between plants Euphydryas chalcedona with C3 and C4 photosynthesis, but also can vary among Euphydryas chalcedona (Nymphalidae: Nymphalinae; plants sharing a photosynthetic mode (O’Leary 1981, Melitaeini) is a univoltine butterfly distributed through- 1988). Thus, it can be a powerful tracer of carbon flow out western North America. Individuals were field from multiple plant sources. Natural abundances of light collected as 5th and 6th instar larvae from Scrophularia stable isotopes are a well-established tracer of nutrient californicus and Mimulus aurantiacus at the Silver Creek flow, within both organisms (Metges et al. 1990, Hobson Hills Butterfly Reserve near San Jose, California, USA. et al. 1997, Schmidt et al. 1999) and ecosystems Larvae were placed in mesh bags on potted S. californi- (Rounick and Winterbourn 1986, Peterson and Fry cus for the remainder of their larval development, and 1987, Ostrom et al. 1997, Wolf and Martı´nez del Rio bags were moved as needed to ensure a constant supply 2000). In a previous study, O’Brien and colleagues (2000) of fresh leaves. Pupae were stored at 208C until adults used carbon isotopes to trace the use of larval and adult emerged. Average female forewing length was 29.89/0.4 diets in reproduction by a hawkmoth. Females were fed mm. Females mated either the day of emergence or the one of two sucrose-based adult diets made from beet day following. Once mated, females were placed in wire (C3) or cane (C4) sugar, both of which differed from the mesh cages (20/20/30 cm) and provided fresh S. natural larval hostplant in 13C content. This approach californicus leaves for oviposition. Females oviposited 280 OIKOS 105:2 (2004) daily or every other day in clusters of typically 100Á/200 to resemble Psiguria umbrosa flowers, and sugar solu- eggs (all other species laid eggs singly). Females were tions were changed daily. Although H. charitonia handfed twice daily. Of the 10 females to successfully normally supplement their diet with pollen, females in mate and start the experiment, 2 were removed because this experiment were not provided with pollen. Eggs they either waited unusually long to oviposit, or didn’t were collected daily. Nine females initiated oviposition eat consistently. The remaining 8 butterflies were used in and were used in isotope measurements; of those, two both isotope analyses and feeding and fecundity mea- died prematurely (N/7 for lifespan and fecundity surements.
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