Effects of larval starvation and adult diet-derived amino acids on reproduction in a fruit-feeding butterfly

Availability of adequate nutrition is among the most important factors affecting growth, development, and reproduction in animals. In holometabolous insects, diets and nutritional needs change between life stages, with larval storage, and adult feeding and reproduction being linked to one another. In several butterfly species, adult feeding is of fundamental importance to realize the full reproductive potential, primarily due to a prominent role of adult diet-derived carbohydrates. In contrast, the role of adult diet-derived amino acids is still under debate, despite the fact that butterflies were often found to preferentially feed on amino acid-rich substrates. Recently it was found that amino acids from adult income could compensate for adverse effects of larval food quality. In our study on the tropical butterfly Bicyclus anynana (Butler) (Lepidoptera: Nymphalidae), we used larval starvation to investigate corresponding effects on female reproductive output. Short periods of larval starvation prolonged development time and reduced larval survival, larval growth rate, pupal mass, and egg size. Regardless of the degree of larval starvation, access to amino acids in the adult diet increased egg size, whereas egg number remained largely unaffected. Thus, although there was some evidence for adult diet-derived amino acids being overall beneficial to reproduction, there was no indication that they can compensate for larval starvation.     

Allocation of resources to reproduction in Styrax obassia in a masting year

An analysis is presented of three possible pathways of reproductive allocation, namely, allocation of resources to reproductive organs from reproductive shoots, from non-reproductive shoots and from the main trunk. These pathways were examined by comparing the amount of storage starch in reproductive shoots, non-reproductive shoots and the main trunk in Styrax obassia, a typical masting tree species, during a year of little flowering (1999) and in a mass-flowering year (2000). In addition, we measured rates of light-saturated photosynthesis in leaves of reproductive and non-reproductive shoots to examine the contribution of photosynthetic production to reproductive costs. In both the main trunk and non-reproductive shoots the pattern of seasonal variation in the amount of starch did not differ between 1999 and 2000. However, in the mass-flowering year, the amount of starch in the reproductive shoots was less than that in non-reproductive shoots during the growing season. Thus, reproductive shoots bore most of the cost of reproduction, although non-reproductive shoots and the main trunk also bore some of the cost. Mass-based rates of light-saturated photosynthesis of the leaves of reproductive shoots were significantly higher than those of non-reproductive shoots during both the flowering and the fruiting period. However, leaves of reproductive shoots had a significantly smaller area, a lower mass per area, and lower concentrations of nitrogen than leaves of non-reproductive shoots, although the number of leaves did not differ between the two types of shoots. Therefore, the amount of photosynthate per shoot was significantly lower in reproductive shoots than in non-reproductive shoots. These results suggest that the cost of reproduction depends predominantly on storage starch in reproductive shoots, although it is still unclear how much photosynthate is allocated to reproductive organs from non-reproductive shoots.     

Resource allocation to reproduction and soma in Drosophila: a stable isotope analysis of carbon from dietary sugar

Metabolic resources in adults of holometabolous insects may derive either from larval or adult feeding. In Drosophila melanogaster, reproduction and lifespan are differently affected by larval vs. adult resource availability, and it is unknown how larval vs. adult acquired nutrients are differentially allocated to somatic and reproductive function. Here we describe the allocation of carbon derived from dietary sugar in aging female D. melanogaster. Larval and adult flies were fed diets contrasting in sucrose (13)C/(12)C, from which we determined the extent to which carbon acquired at each stage contributed to adult somatic tissue and to egg manufacture. Dietary sugar is very important in egg provisioning; at every age, roughly one half of the carbon in eggs was derived from sugar, which turned over from predominantly larval to entirely adult dietary sources. Sucrose provided approximately 40% of total somatic carbon, of which adult dietary sucrose came to supply approximately 75%. Unlike in eggs, however, adult acquired sucrose did not entirely replace the somatic carbon from larvally acquired sucrose. Because carbon from larval sucrose appears to be fairly "replaceable", larval sucrose cannot be a limiting substrate in resource allocation between reproduction and lifespan.     

Effects of adult nutrition on female reproduction in a fruit-feeding butterfly: the role of fruit decay and dietary lipids

It was generally believed that butterflies and other holometabolous insects rely primarily on reserves accumulated during the larval stage for reproduction. Recent studies, however, highlight the often fundamental importance of adult nutrition to realize the full reproductive potential. While the importance of carbohydrates is fairly well understood, the role of most other adult-derived substances is only partially resolved. We here focus on the effects of dietary lipids (cholesterol, polyunsaturated fatty acids) and fruit decay (dietary yeast, ethanol) on female reproduction in the tropical, fruit-feeding butterfly Bicyclus anynana (Nymphalidae). We found that banana-fed control females outperformed all other groups fed on sucrose-based diets. Lipids, yeast or ethanol added to a sugar solution did not yield a similarly high reproductive output compared to fruit-fed females. Groups fed fresh or decaying banana showed no differences in reproductive performance. As we could not identify a single pivotal substance, we conclude that resource congruence (the use of nutrient types in a specified ratio) rather than any specific nutrient component is of key importance for maximum reproductive output. Further, dietary quality may affect egg hatching success in spite of no obvious effects on egg size and number. Thus, any implications about potential fitness effects of different diets need to consider egg (and hatchling) viability in addition to fecundity.     

Effects of adult-derived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly

It is generally believed that butterflies (and other holometabolous insects) rely primarily on reserves accumulated during the larval stage for reproduction, whereas the carbohydrate-rich adult diet is thought to mainly cover energy requirements. In at least some species though, realization of the full reproductive potential is extensively affected by post-eclosion nutrition. While the importance of carbohydrates is fairly well understood, the role of adult-derived amino acids and micronutrients is controversial and largely unknown, respectively. We here focus on the effects of different adult diets on female reproduction in the tropical, fruit-feeding butterfly Bicyclus anynana (Nymphalidae). Carbohydrates were the most important adult-derived nutrients affecting reproduction. Adding amino acids, vitamins or minerals to sucrose-based solutions did not yield a reproductive output equivalent to that of fruit-fed females, which showed the highest performance throughout. This suggests that either not yet identified compounds of fruit substantially contribute to reproduction, or that resource congruence (the use of nutrient types in a specified ratio) rather than any specific nutrient component is of key importance. Apart from adult income, realized fecundity depended on egg size and longevity, with the former dominating when dietary quality was low, but the latter when quality was high. Thus, the egg size-number trade-off seems to be affected by female nutrition.     

Estuarine recruitment of a marine goby reconstructed with an isotopic clock

Information on movement patterns of marine fishes between estuarine populations and stocks at sea is fundamental to understanding their population dynamics, life history tactics and behavior. Furthermore, understanding estuarine habitat use by marine fishes is crucial for their effective conservation and integrated estuarine management. Although large numbers of young marine fish make use of temperate estuaries in highly predictable abundance patterns, very little is known about how estuarine populations interact with the populations at sea. Recruitment of sand goby Pomatoschistus minutus (Pallas, 1770) into the low salinity zone of the Scheldt estuary (Belgium) was reconstructed over an entire year by means of an isotopic clock. These results were combined with a growth model to yield age and length at immigration. Sand gobies entered the upper Scheldt estuary almost continuously from May onwards, except in July when they appeared to avoid the estuary due to warm summer temperatures. About 70% of the fish caught in the upper estuary resided there for less than 1 month, which indicates a strong temporal overlap of immigration and emigration. This complex migration pattern suggests that estuarine residence is caused by trade-offs made at the individual level, whereby migration is probably triggered by temperature. The high turnover of individuals in the estuarine population leads us to question the functional role of the estuary for marine fishes. Sand gobies entering the upper estuary had a wide range of ages and body sizes, although they were at least 2 months old and had a minimum standard length of approximately 20 mm. This study shows that the use of an isotopic clock strongly complements catch data and is useful to describe the connectivity between populations.     

Plant response to variations in nitrogen availability in a desert shrubland community

Spatial variations in nitrogen availability were studied in a desert community codominated byLarrea tridentata (DC.) Cov. andProsopis glandulosa Torr. Measurements of natural ¹⁵N values in tissues suggested thatProsopis obtains approximately half of its nitrogen through direct symbiotic fixation. Soils were collected under 1)Prosopis shrubs, 2)Larrea shrubs 2 m fromProsopis (LP), and 3)Larrea 2 m from otherLarrea but> 5 m from the nearestProsopis (LL).Prosopis soils showed significantly higher rates of nitrogen mineralization than LL soils in both A and B horizons. Rates of mineralization in LP soils were significantly higher than rates in LL soils only in the B horizon and were not significantly different from rates inProsopis soils. Leaf nitrogen concentrations were significantly higher in LP shrubs (2.06%) than in LL shrubs (1.78%), although ¹⁵N values did not differ between the two shrub types. Nitrogen concentrations inPerezia nana Gray, a perennial herb, were greater in plants underProsopis shrubs (2.09%) than under LP shrubs (1.93%) or LL shrubs (1.67%). Despite apparent differences in nitrogen availability, biomass ofLarrea and density ofPerezia did not differ significantly among these sites.     

Multidimensional stable isotope analysis illuminates resource partitioning in a sub‐Antarctic island bird community

A central theme in community ecology is understanding how similar species co‐exist and how their interactions may evolve in the context of climate change. Most studies of resource partitioning among central place foragers, particularly birds, focus on the offspring‐rearing period, when they are accessible, but breeding success may be determined earlier and little is known about how such species partition resources at the onset of breeding. We used a non‐invasive approach to evaluate resource partitioning in co‐existing females at a sub‐Antarctic island during their pre‐laying periods. Three hypotheses were tested using carbon, nitrogen and oxygen stable isotope ratios measured in shells and membranes of hatched eggs as ecological tracers: 1) resource partitioning by geographic location and trophic level will exist among the 12 bird species and will be enhanced within taxonomic groups; 2) given the absence of strong oxygen gradients in the Southern Ocean we will not detect spatial structuring based on oxygen isotopes, but differences will exist between resident and oceanic species as the former may use meteoric water; 3) capital and income breeder strategies can be differentiated using stable isotopes of egg remains. Two and three dimensional isotopic data showed resource partitioning among species. As predicted, segregation was evident within the four main taxonomic groups: penguins, albatrosses, burrowing petrels and giant petrels. Unexpectedly, oxygen isotopes revealed widespread use of meteoric water among a suite of sub‐Antarctic birds. Stable isotopes allowed us to identify females of most species as income breeders at the onset of breeding, with the exception of the females of the two crested penguin exhibiting a mix of income and capital resources use. Multidimensional isotopic analyses revealed that resource partitioning exists at multiple stages of the annual cycle in ways likely to be important under global change, exhibiting wide potential for ecosystem analysis.     

Feeding responses and food preferences in the tropical, fruit-feeding butterfly, Bicyclus anynana

In the tropical butterfly Bicyclus anynana (Nymphalidae) essential components of fitness (such as fecundity and longevity) depend to a large degree on exogenous adult-derived nutrients, particularly carbohydrates. We investigated which of the nutrients/compounds found in the adult diet act as feeding stimuli, and whether butterflies show preferences for particular nutrients or combinations. Only sugars and alcohols acted as feeding stimuli, the highest responses being found for sucrose, glucose, ethanol, butanol and propanol. Various other compounds (e.g. amino acids, acetic acid, vitamins, lipids, salts, and yeast) did not elicit any probing or feeding responses. Behavioural tests revealed a clear preference hierarchy for sugars (sucrose > glucose > fructose > maltose), but not for alcohols. Butterflies did not discriminate between sucrose solutions enriched with different nutrients and plain sucrose solutions, although they showed a preference for acetic acid and an aversion to salts and ascorbic acid when offered in combination with sucrose. Throughout, both sexes showed very similar patterns. We conclude that locating carbohydrate sources seems sufficient to cover all the butterflies’ nutritional needs, while alcohols function primarily as long range signals, guiding the butterflies to food sources. Thus, fruit-feeding butterflies, in contrast to nectar-feeding butterflies, appear not to have distinctive preferences for e.g. amino acids or salts, but do share a common primary preference for sucrose.     

Trophic structure of macro- and meso-invertebrates in Japanese coniferous forest: Carbon and nitrogen stable isotopes analyses

Few studies have been published on the feeding ecology of Japanese soil fauna based on stable isotope analysis. Therefore, the present work aims to use this technique for studying the trophic structure of Japanese soil fauna at two coniferous forests. Significant differences were observed between investigated sites (Arahama and Gamo) in genus richness and abundance, while for Shannon diversity indexes the difference was non-significant. The isotopic signatures (δ¹³C and δ¹⁵N) of the invertebrates collected at Arahama ranged from 0.3 to 6.3‰ for δ¹⁵N and from −27.3 to −23.3‰ for δ¹³C. At Gamo, invertebrates δ¹³C values ranged from −26.1 to −23.5‰ and δ¹⁵N values ranged from 1.6 to 6.8‰. At both sites, invertebrates formed two distinct groups on the basis of combined C and N stable isotope ratios. The locations of these groups related to δ¹³C values. The less enriched group (δ¹³C < −25‰) and the more enriched one (δ¹³C > −25‰). The range of δ¹⁵N for the present animals exceeded two trophic levels. While, the gradual ¹⁵N enrichment within the invertebrates species may indicate the dominance of omnivory in soil food webs. The differences between sites in δ¹⁵N confirm the importance of studying the trophic structure of soil fauna locally.     

Cost of reproduction in males of a satyrine butterfly Lethe diana

Adult butterflies feed largely on floral nectar and tree sap, both of which consist mainly of carbohydrates and include little nitrogen. They depend on the larval diet for nitrogenous resources. Consequently, there is a trade‐off between the reproductive and somatic nitrogenous investments of adults. Furthermore, male butterflies invest a considerable amount into spermatophores, containing nitrogen, which they give to their sexual partners. One way in which male butterflies could potentially replenish their spermatophores is by flight muscle histolysis, which may reduce locomotor ability and lifespan. In the present study, the effect of mating experience on nitrogen dynamics and the lifespan of males is investigated in the satyrine butterfly Lethe diana (Butler). Mated males do not have less thoracic nitrogen than virgin males, suggesting that mating experiences do not induce spermatophore recovery through flight muscle histolysis. Mated males possess less abdominal nitrogen than virgin males at death, indicating that they cannot recover the lost nitrogenous resource used for a single mating. Lifespan does not differ between mated and virgin males. Thus, reproduction and longevity are not fuelled necessarily by the same shared resource pools. Spermatophore mass increases as males get older. Considering that resources for producing spermatophores are limited, males may adjust the spermatophore mass strategically, depending on their chances of future reproduction.     

Carbon fluxes to the soil in a mature temperate forest assessed by <Superscript>13</Superscript>C isotope tracing

Photosynthetic carbon uptake and respiratory C release from soil are major components of the global carbon balance. The use of ¹³C depleted CO₂ (¹³C = –30) in a free air CO₂ enrichment experiment in a mature deciduous forest permitted us to trace the carbon transfer from tree crowns to the rhizosphere of 100–120 years old trees. During the first season of CO₂ enrichment the CO₂ released from soil originated substantially from concurrent assimilation. The small contribution of recent carbon in fine roots suggests a much slower fine root turnover than is often assumed.¹³C abundance in soil air correlated best with temperature data taken from 4 to 10 days before air sampling time and is thus rapidly available for root and rhizosphere respiration. The spatial variability of ¹³C in soil air showed relationships to above ground tree types such as conifers versus broad-leaved trees. Considering the complexity and strong overlap of roots from different individuals in a forest, this finding opens an exciting new possibility of associating respiration with different species. What might be seen as signal noise does in fact contain valuable information on the spatial heterogeneity of tree-soil interaction.     

The importance of small scales to the fruit-feeding butterfly assemblages in a fragmented landscape

Nowadays 37% of Earth’s ice-free land is composed by fragments of natural habitats settled in anthropogenic biomes. Therefore, we have to improve our knowledge about distribution of organisms in remnants and to understand how the matrix affects these distributions. In this way, the present study aims to describe the structure of the butterfly assemblages and determined how richness and abundance are influenced by the scale of the surrounding vegetation. General linear models were used to investigate how the type and scale of vegetation cover within a radius of 100–2,000 m around the sampling point explained butterfly diversity. After sampling ten forest fragments we found 6,488 individuals of 73 species. For all clades tested null models explain the species richness at the fragments better than other models when we include the effect of butterfly abundance as a covariate. Abundance of Satyrini, Brassolini, and Biblidinae were best predicted by small scales (100–200 m), and large scales were more suited for Charaxinae. The presence of pasture best explains the abundance of all groups except Charaxinae, which was best explained by early-regrowth forest. The abundance of different species and groups are correlated with different kinds of vegetation cover. However, we demonstrate that small scales (100–200 m) are more effective at explaining the abundance of most butterflies. These results strongly suggest that efforts to preserve insect diversity in forest fragments should take in account the immediate surroundings of the fragment, and not only the regional landscape as a whole. In general, actions of people living near forest fragments are as important to fruit-feeding butterflies as large scale actions are, with the former being seldom specified in management plans or conservation policies.     

Asymmetric Contribution of Isotopically Contrasting Food Sources to Vertebrate Consumers in a Subtropical Semi‐arid Ecosystem

Habitat heterogeneity is a primary ecological factor that is particularly pronounced in arid ecosystems. The Tehuacán valley is a subtropical semi‐arid ecosystem in which several species of columnar cacti and agave (i.e., CAM plants) constitute the dominant elements accompanied by patches of trees and shrubs (i.e., C₃ plants). Vegetation in Tehuacán is isotopically heterogenous because CAM plants have less depleted δ¹³C values than C₃ plants. Fruits and flowers of cactus and agaves offer abundant food to vertebrates, but their leaves might be less attractive to insects than the leaves of C₃ plants. Therefore, we use carbon and nitrogen stable isotope analysis to test the hypothesis that C₃ and CAM food would contribute asymmetrically to different guilds of birds and bats. We predict that granivorous and frugivorous birds and nectarivorous and frugivorous bats will consume a CAM diet, whereas insectivorous birds and bats will consume a C₃ diet. Due to omnivory of bird and bat consumers, we predict that the importance of CAM food will decrease as the trophic level of the animal increases. Our results showed that CAM food predominated in plant‐eating birds and in some flower‐visiting bats, whereas C₃ food predominated in insect‐eating bats and birds and frugivorous bats. Habitat heterogeneity in Tehuacán is important for conservation due to the asymmetric role of CAM and C₃ food in the nutrition of different feeding guilds of vertebrates. Our study provides basic information to evaluate the potential impact of habitat loss on functional groups of consumers in a semi‐arid ecosystem.     

Brief communication: Tissue isotopic enrichment associated with growth depression in a pig: Implications for archaeology and ecology

Stressors such as fasting or poor diet quality are thought to potentially alter the nitrogen and carbon isotopic values of animal tissues. In this study, we demonstrate an inverse correlation between growth rate and multiple tissue enrichment of δ¹⁵N, δ¹³C, and, to a lesser degree, δ¹⁸O in a juvenile pig. A more complex pattern is observed with respect to tissue δD and growth rate. The observed association between growth rate and tissue isotopic fractionation has important implications for paleodietary and migratory reconstructions of archaeological populations that may have been affected by famine, malnutrition, seasonal variation in food availability, and/or other factors that can affect childhood growth rates. Am J Phys Anthropol 2010. © 2010 Wiley‐Liss, Inc.     

Factors controlling the stable isotope composition and C:N ratio of seston and periphyton in shallow lake mesocosms with contrasting nutrient loadings and temperatures

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