Does diet breadth control herbivorous insect distribution size? Life history and resource outlets for specialist butterflies

Although butterfly distributions are known to be positively correlated with the number of larval hostplants used it is not known to what extent larval hostplant number uniquely influences butterfly distributions and to what extent effects are indirect through other variables. This issue is central to understanding the part generalism and specialism in host use play in organism persistence and conservation. Here, we have modelled the links between larval hostplant number and butterfly distributions using data from the UK. The model identifies the key variables that connect number of hostplants used by butterflies and the size of butterfly distributions. Significant correlations between variables give support to the model. Access to more hostplants is shown to affect a number of resource and life history variables impinging on butterfly population abundances and butterfly distributions. Butterfly distributions are largely accounted for (R²>81%) by a set of resource and life history variables linked to numbers of hostplants: biotope occupancy, nectar sources used, utilities (the number of structures used by each life-cycle stage) and hostplant abundance. Application of partial regression demonstrates that the unique contribution of hostplant number to butterfly distributions is relatively small (R² = 14% to 33%), indicating that host use generalism has a limited direct impact on distributions. The modest correlations linking variables within the model illustrates that specialist phytophage feeders have a number of potential, distinct outlets, via resource and life history variables, to compensate for lack of supplementary larval hosts within their geographical ranges and enabling them to persist. Variables in the model each have considerable independence of action; without this, specialist feeders would have difficulty in expanding their distributions and acquiring new hosts, functionally-linked processes affecting evolutionary dynamics and persistence. We also question the nature of a direct functional link between local population abundance and distributions. Our model suggests a more complex functional relationship with implications for conserving insect herbivores.     

The scale of resource specialization and the distribution and abundance of lycaenid butterflies

Numerous hypotheses have been proposed for the commonly observed, positive relationship between local abundance and geographic distribution in groups of closely related species. Here I consider how hostplant specialization and abundance affect the relative abundance and distribution of lycaenid butterflies (Lepidoptera: Lycaenidae). I first discuss three components of specialization: local specialization, turnover of specialization across a species’ range, and the minimum number of resources (or habitats) required by a species. Within this framework, I then consider one dimension of a lycaenid species’ niche, larval hostplant specialization. In a subalpine region of Colorado, I surveyed 11 lycaenid species and their hostplants at 17 sites. I compare this local information to continental hostplant use and large-scale distributions of the lycaenids and their hostplants. Local abundance of a lycaenid species is positively correlated with its local distribution (the number of sites occupied), but not with its regional or continental distribution. Neither local specialization (the number of hostplants used within one habitat) nor continental specialization (the number of hostplants used across many habitats) is correlated with local lycaenid abundance. Continental specialization is positively correlated with a species’ continental distribution, however. Finally, while generalist butterflies tend to have more hostplant available to them, differences in resource availability do not explain the differences in butterfly abundance. Although local abundance is correlated only with local distribution, I suggest that abundance-distribution relationships might emerge at regional and continental scales if local abundance were averaged across many habitat types. Consideration of the scale of a species’ resource specialization (within or among habitats) appears to be key to understanding the relationships between resource specialization, resource availability, and a species’ abundance and distribution. Received: 1 September 1999 / Accepted: 12 December 1999     

Conserving a wetland butterfly: quantifying early lifestage survival through seasonal flooding, adult nectar, and habitat preference

Conservation of once thought extinct populations of Lycaena xanthoides in western Oregon will require specific information of how the butterfly interacts with its now rare wetland habitat. Three experiments were conducted to yield information directly applicable to wetland restoration work: (1) to quantify the survival of L. xanthoides eggs laid on inundated plants, (2) to quantify adult nectar preferences, (3) to investigate the role of adult resources and how butterflies assess habitat quality. Survival of eggs laid on inundated plants was nearly seven times lower than the survival of eggs laid on uninundated plants, indicating that eggs laid on plants that are seasonally flooded are a population sink. Adult L. xanthoides preferred an endemic native nectar plant, Grindelia integrifolia × nana, as an adult resource and used it approximately 88% of the time while other butterfly species preferred to nectar on the non-native Mentha pulegium. Adult L. xanthoides had a significantly greater short-term recapture rate in two restored study sites that had a high relative amount of Grindelia integrifolia × nana compared to a degraded site that lacked the preferred nectar source. Based on the results from the three small experiments, restoration of wetlands for L. xanthoides should concentrate plantings of host plant in non-flooded areas and propagate conspicuous patches of the preferred nectar plant.     

Foraging in nature: Contrasting responses to resource heterogeneity at small‐ and large‐spatial scales

A key problem faced by foragers is how to forage when resources are distributed heterogeneously in space. This heterogeneity and associated trade‐offs may change with spatial scale. Furthermore, foragers may also have to optimize acquiring multiple resources. Such complexity of decision‐making while foraging is poorly understood. We studied the butterfly Ypthima huebneri to examine how foraging decisions of adults are influenced by spatial scale and multiple resources. We predicted that, at a small‐spatial scale, the time spent foraging in a patch should be proportional to resources in the patch, but at large‐spatial scales, due to limitations arising from large travel costs, this relationship should turn negative. We also predicted that both adult and larval resources should jointly affect foraging butterflies. To test these predictions, we laid eleven plots and sub‐divided them into patches. We mapped nectar and larval resources and measured butterfly behavior in these patches and plots. We found that adult foraging behavior showed contrasting relationships with adult resource density at small versus large‐spatial scales. At the smaller‐spatial scale, butterflies spent more time feeding in resource‐rich patches, whereas at the large‐scale, butterflies spent more time feeding in resource‐poor plots. Furthermore, both adult and larval resources appeared to affect foraging decisions, suggesting that individuals may optimize search costs for different resources. Overall, our findings suggest that the variation in foraging behavior seen in foragers might result from animals responding to complex ecological conditions, such as resource heterogeneity at multiple spatial scales and the challenges of tracking multiple resources.     

Nectar Resources and Their Influence on Butterfly Communities on Reclaimed Coal Surface Mines

Despite the critical role insects play in ecosystem functioning, there has been little study of factors affecting their reestablishment in restored ecosystems. The goals of this research were to quantify the nectar resources provided by reclaimed coal surface mines and to examine the role nectar resources play in determining butterfly community composition on these sites. Adult butterfly communities and nectar resources were sampled on 18 reclaimed coal surface-mined sites and five unmined hardwood sites in southwestern Virginia. Recently, reclaimed sites provided an average of 300 times the nectar abundance of the surrounding hardwoods, and nectar abundance and species richness decreased with time since reclamation. Total nectar abundance was highly correlated with total butterfly abundance and species richness for the entire flight season; these variables were also significantly correlated among sites during most of the 12 sampling periods during the flight season. In only a few cases, however, were butterfly and nectar abundance and species richness significantly correlated within individual sites during the flight season. These results suggest that, although adults of many butterfly species move in response to nectar availability, nectar resources are not sufficiently limiting that their life histories have evolved to maximize nectar resources temporally. While planting species in restored areas that provide abundant nectar will likely attract adult butterflies, this is only one of a number of habitat variables that must be considered in efforts to restore butterfly populations. Finally, adult butterflies appear to have limited utility as indicators of revegetation success.     

Just how important are structural elements as habitat components? Indications from a declining lycaenid butterfly with priority conservation status

Recently, it has been suggested that habitats for insect herbivores have been too narrowly defined, often on the basis of larval hostplants; in particular, non-consumable resources (called utilities; structural elements) have been ignored. Here, the importance of utility resources for roosting and mate location has been examined in the silver-studded blue butterfly Plebejus argus (L.) (Lycaenidae) on the Great Ormes Head, North Wales, UK. The methods included using dedicated surveys and correspondence analysis applied to behavioural observations in relation to vegetation structure on a transect through a key patch for this metapopulation model species. A substantial and significant bias in roosting (97%) and mating (75%) is found to occur outside hostplant areas on shrubs and rank bunched grasses and forbs. Population density is higher in shrubby areas and shrubs are increasingly occupied during the afternoons and night, during the late flight season and in cloudy, cool and windy weather. These findings suggest that shrubs are a valuable habitat component for this butterfly, at least at this coastal location, and important for their conservation. As scrub growth is inimical to calcicolous grassland, population status will depend on a fine balance between shrub and hostplant cover dependent on grazing and browsing by the indigenous goat, sheep and rabbit populations as well as on controlled cutting and burning. Opportunities exist for increasing population size and distribution on the headland but this will need to be managed carefully. There are also implications for metapopulation dynamics studies; the status of shrubs neighbouring host plant areas switches from that of barriers to resources and refuges.     

Similarity and specialization of the larval versus adult diet of European butterflies and moths

Many herbivorous insects feed on plant tissues as larvae but use other resources as adults. Adult nectar feeding is an important component of the diet of many adult herbivores, but few studies have compared adult and larval feeding for broad groups of insects. We compiled a data set of larval host use and adult nectar sources for 995 butterfly and moth species (Lepidoptera) in central Europe. Using a phylogenetic generalized least squares approach, we found that those Lepidoptera that fed on a wide range of plant species as larvae were also nectar feeding on a wide range of plant species as adults. Lepidoptera that lack functional mouthparts as adults used more plant species as larval hosts, on average, than did Lepidoptera with adult mouthparts. We found that 54% of Lepidoptera include their larval host as a nectar source. By creating null models that described the similarity between larval and adult nectar sources, we furthermore showed that Lepidoptera nectar feed on their larval host more than would be expected if they fed at random on available nectar sources. Despite nutritional differences between plant tissue and nectar, we show that there are similarities between adult and larval feeding in Lepidoptera. This suggests that either behavioral or digestive constraints are retained throughout the life cycle of holometabolous herbivores, which affects host breadth and identity.     

Natural selection on body size is mediated by multiple interacting factors: a comparison of beetle populations varying naturally and experimentally in body size

Body size varies considerably among species and among populations within species, exhibiting many repeatable patterns. However, which sources of selection generate geographic patterns, and which components of fitness mediate evolution of body size, are not well understood. For many animals, resource quality and intraspecific competition may mediate selection on body size producing large-scale geographic patterns. In two sequential experiments, we examine how variation in larval competition and resource quality (seed size) affects the fitness consequences of variation in body size in a scramble-competing seed-feeding beetle, Stator limbatus. Specifically, we compared fitness components among three natural populations of S. limbatus that vary in body size, and then among three lineages of beetles derived from a single base population artificially selected to vary in size, all reared on three sizes of seeds at variable larval density. The effects of larval competition and seed size on larval survival and development time were similar for larger versus smaller beetles. However, larger-bodied beetles suffered a greater reduction in adult body mass with decreasing seed size and increasing larval density; the relative advantage of being large decreased with decreasing seed size and increasing larval density. There were highly significant interactions between the effects of seed size and larval density on body size, and a significant three-way interaction (population-by-density-by-seed size), indicating that environmental effects on the fitness consequences of being large are nonadditive. Our study demonstrates how multiple ecological variables (resource availability and resource competition) interact to affect organismal fitness components, and that such interactions can mediate natural selection on body size. Studying individual factors influencing selection on body size may lead to misleading results given the potential for nonlinear interactions among selective agents.     

蝴蝶在生境和生物小区之间的移位伴随着对外来蜜源的利用

在发育成熟的温带环境中,植食性昆虫群落能迅速适应引入植物并将其作为幼虫的食物和花蜜.我们研究了经过森林砍伐的热带环境中蝴蝶对利用引入植物作为蜜源植物的适应快慢程度,并研究了蝴蝶-显花植物在新的生物小区中出现的范围,发现蝴蝶对引入显花植物的利用和探访多于本地植物,这与引入植物在调查地点、生物小区和植物丰度中的普遍性有关.此外,取食花蜜的蝴蝶和显花植物与正在形成的的生物小区有关,例如路边、农田、集约耕地以及花园.在这些新生物小区中,引入植物很重要,因为它们为蝴蝶提供了蜜源.     

Estimating female reproductive success of a threatened butterfly: influence of emergence time and hostplant phenology

We estimated lifetime reproductive success of Euphydryas editha bayensis (Nymphalidae), a federally listed threatened butterfly, based on age-specific fecundity and both adult and offspring survival. Our results indicate that the relative timing of adult emergence and larval hosplant senescence strongly influenced reproductive success of females. For 1992, we estimated that only 8–21% of the eggs laid by females emerging on the 1st day of the 4-week flight season would produce larvae that reach diapause. This figure dropped to 1–5% for females emerging 7 days into the flight season. Within our entire sample, we estimated that 64–88% of the females produced offspring with less than a 2% probability of reaching diapause. These estimates are particularly striking given that they are based on only one source of larval mortality — prediapause starvation due to hostplant senescence. This dependence of reproductive success on the relative timing of female emergence and hostplant senescence may reduce effective population size and render E. editha bayensis especially vulnerable to local extinction events.     

Microclimatic buffering and resource‐based habitat in a glacial relict butterfly: significance for conservation under climate change

In contrast to several organisms that have already shown range shifts to the north as a response to climate change, southern populations of relict species are trapped in isolated altitudinal habitats. Therefore, there is a growing interest to better understand their habitat use, with particular attention to the thermal aspects and associated significance for their habitat management. We address this issue by a study of larval habitat use relative to vegetation structure and microclimate in a glacial relict butterfly of peat bog ecosystems, using a functional, resource‐based habitat approach. We analysed caterpillar presence and density relative to vegetation composition (reflecting gradients of humidity, temperature, and natural succession of the peat bog) and to the availability and quality of thermal refuges for caterpillars (i.e., structures provided by Sphagnum hummocks). We also tested caterpillar survival rates under different temperature and humidity treatments. We found that (1) Boloria aquilonaris was a specialist butterfly of early successional stages with very humid zones of peat bog, (2) the lack of Sphagnum hummocks reduced larval habitat suitability, and hence the population density, and (3) a reduction of the thermal buffering ability of Sphagnum hummocks was observed in less humid, degraded parts, or late‐successional stages of peat bog. A larval rearing experiment showed a significant impact of temperature on caterpillar survival; survival being higher at lower temperature. Our field and laboratory results support the idea that the thermal environment exploited by caterpillars should be considered as a functional resource and included in a population‐specific habitat definition. Appropriate management of the peat bog habitat of this glacial relict species should not exclusively focus on the larval and adult feeding resources, but also on the quality of thermal refuges provided by Sphagnum hummocks in humid zones of the peat bog, especially in the current critical context of climate warming.     

Enhancing offspring quality or quantity? Different ways for using nectar amino acids in female butterflies

Butterfly-pollinated flowers offer nectar with higher amino acid concentrations than most flowers pollinated by other animals, and female butterflies of some species prefer to consume amino acid-rich nectar. However, for over 30 years, there has been an ongoing discussion about whether nectar amino acids benefit butterfly fitness. A clear positive effect was only shown for the nectar-feeding Araschnia levana, and females of the fruit-feeding Bicyclus anynana also increased offspring quality when they were fed amino acids as adults. Thus, severe doubts remain about the general significance of these single positive results. We therefore tested a further species from a phylogenetically different butterfly subfamily, the small heath (Coenonympha pamphilus L., Satyrinae), taking into account feeding conditions over the whole life cycle of this species. C. pamphilus females receiving nectar amino acids as adults, irrespective of larval food quality, produced heavier larvae and also increased the hatching success of their eggs over the oviposition period. Furthermore, females raised under nitrogen-poor larval conditions tended to use nectar amino acids to increase the number of eggs laid. Thus, C. pamphilus females used nectar amino acids primarily to increase their offspring quality, and secondly tended to increase offspring quantity, if larval resources were scarce, showing a resource allocation pattern differing from both B. anynana and A. levana. Our study supports the old postulate that nectar amino acids generally enhance butterfly fitness.     

Linking nectar amino acids to fitness in female butterflies

Nectar of butterfly-pollinated flowers contains generally higher levels of amino acids than does nectar of flowers pollinated by most other animal types. One proposed explanation is that these amino acids promote butterfly fitness, although the evidence has been equivocal. In a new study, Mevi-Schütz and Erhardt showed that nectar amino acids enhanced fecundity in the butterfly Araschnia levana, but only when the larval diet was poor. Their results support the hypothesis that butterflies are agents of selection for higher nectar amino acid production, suggest that the larval food plant has a key role in the evolution of the flower-butterfly mutualism, and demonstrate that the importance, to butterfly reproduction, of different nutrient sources varies with butterfly nutritional state.     

Robustness and uncertainty in estimates of butterfly abundance from transect counts

Many butterfly populations are monitored by counting the number of butterflies observed while walking transects during the butterfly’s flight season. Methods for estimating population abundance from these transect counts are appealing because they allow rare populations to be monitored without capture–recapture studies that could harm fragile individuals. An increasingly popular method for estimating abundance from transect counts relies on strong assumptions about the counting process and the processes that govern butterfly population dynamics. Here, we study the statistical performance of this method when underlying model assumptions are violated. We find that estimates of population size are robust to departures from underlying model assumptions, but that the uncertainty in these estimates (i.e., confidence intervals) is substantially underestimated. Alternative bootstrap and Bayesian methods provide better measures of the uncertainty in estimated population size, but are conditional upon knowledge of butterfly detectability. Because of these requirements, a mixed approach that combines data from small capture–recapture studies with transect counts strikes the best balance between accurate monitoring and minimal injury to individuals. Our study is motivated by monitoring studies for St. Francis satyr (Neonympha mitchelli francisci), a rare and relatively immobile butterfly occurring only in the sandhills region of south-central North Carolina, USA.     

Structure and function of a non-interactive, reactive insect-plant system

Rhagoletis alternata is a common tephritid fly in central Europe, whose larvae feed on the hypanthium of rose hips. The resource-consumer system is “non-interactive”, i.e. the insect has little or no impact on host plant fitness and therefore is not able to influence the rate at which larval food resources are renewed. The system is “reactive”, since fluctuations in the carrying capacity (hip density) of the host plant are important for determining year-to-year fluctuations in the insect's population size. Insect fluctuations exceed those of its carrying capacity. The insect's efficient exploitation strategy, maximizing its fitness at high as well as low resource supply, must be attributed to the variable and unpredictable relationship between resource availability and consumer density. The only regulatory mechanism is contest competition when larval densities exceed the carrying capacity. Due to the low impact of the insect, its exploitation strategy is apparently not opposed by mechanisms selecting for defence in the host plant. This lack of defence and the efficient exploitation strategy may be important factors for the frequently observed high degree of the resource utilization by the insect. Received: 3 November 1997 / Accepted: 22 January 1998     

Metapopulation structure and habitat quality in modelling dispersal in the butterfly Iolana iolas

Quantifying dispersal is fundamental to understanding the effects of fragmentation on populations. Although it has been shown that patch and matrix quality can affect dispersal patterns, standard metapopulation models are usually based on the two basic variables, patch area and connectivity. In 2004 we studied migration patterns among 18 habitat patches in central Spain for the butterfly Iolana iolas, using mark–release–recapture methods. We applied the virtual migration (VM) model and estimated the parameters of emigration, immigration and mortality separately for males and females. During parameter estimation and model simulations, we used original and modified patch areas accounting for habitat quality with three different indices. Two indices were based on adult and larval resources (flowers and fruits) and the other one on butterfly density. Based on unmodified areas, our results showed that both sexes were markedly different in their movements and mortality rates. Females emigrated more frequently from patches, but males that emigrated were estimated to move longer daily dispersal distances and suffer higher mortality than females during migration. Males were more likely to emigrate from small than from large patches, but patch area had no significant effect on female emigration. The effects of area on immigration rate and the within-patch mortality were similar in both sexes. Based on modified areas, the estimated parameter values and the model simulation results were similar to those estimated using the unmodified patch areas. One possible reason for the failure to significantly improve the parameter estimates of the VM model is the fact that resource quantity and butterfly population sizes were strongly correlated with patch area. Our results suggest that the standard VM modelling approach, based on patch area and connectivity, can provide a realistic picture of the movement patterns of I. iolas .     

Contrasting resource-dependent responses of hoverfly richness and density to landscape structure

Hoverflies (Diptera: Syrphidae) in agroecosystems have gained much attention recently because the larvae of some species are efficient control agents of crop aphids, and adult hoverflies provide pollination services to wild flowers and flowering crops. We assessed the density and species richness of hoverflies in 32 calcareous grasslands, which constitute a semi-natural habitat for adult hoverflies, by means of six transect walks from April to September 2004. Our results show that local habitat factors and landscape factors influenced hoverfly communities, and that their effects on hoverfly richness and density were quite contrary. Hoverfly species richness was affected by factors related to resource heterogeneity such as species richness of flowering plants, area of grassland habitat, and landscape diversity, which all imply the availability of diverse micro- and macrohabitats for adults and larvae. Hoverfly density, in contrast, depended on factors related to resource quantity, such as the amount of pollen and nectar resources for adults and the amount of larval macrohabitats in the surrounding matrix. Therefore, both adult and larval habitat requirements have to be considered when analysing hoverfly communities in agricultural landscapes. Species guilds responded to specific land-use types such as annual crops and woodland at different spatial scales, indicating variation in species’ mobility and in the degree of spillover effects among neighbouring landscape elements.     

Evidence based conservation of butterflies

Few results of research aimed at solving questions arising from butterfly conservation are rigorously tested by manipulating populations and habitats in the field. Some factors common to successful conservation projects are analysed. In most non-migratory species, population density may vary by up to two orders of magnitude between sites or over time, and is primarily determined by the extent to which a subset of each species’ foodplant (or ant host) exists in the optimum growth-form or micro-habitat preferred by its larvae. Successful conservation projects have identified the optimum subset of each species’ larval resource before managing sites to increase its representation. In contrast, short-term fluctuations around a site’s carrying capacity or equilibrium level are mainly attributable to variation in weather, and are generally two orders of magnitude smaller than that attributable to larval habitat quality. There is little evidence that changing the abundance of adult resources, apart from shelter, influences population size or trends. The main constraint of the adult stage is the inability of many species to track the generation of new habitat patches that arise across modern landscapes. Within-patch larval habitat quality is again critical at the meta-population scale, explaining slightly more examples of patch occupancy than site isolation. This is because the higher density populations supported by optimum habitat are less likely to go extinct, and immigrants to new high-quality patches have a higher probability of founding new populations. Such patches may also generate up to a hundred times more emigrants per hectare than low-quality source patches.     

The impact of urban development on butterflies within a city region

The effect of urban development on butterfly species' richness and species' incidence is tested for the Greater Manchester conurbation and two sample areas, mapped at finer scales, within the southern part of the conurbation. The tests include measures of bias for recording effort (number of visits). Species' richness is found to increase with percentage urban cover for Greater Manchester (tetrad scale) and decrease with urban cover for the two sample areas in South West Manchester (1 km scale) and the Mersey Valley (100 m scale). For Greater Manchester, the increase in species' richness with increased urban cover is largely explained by lower species' richness at higher altitude in the Pennines bounding the conurbation. For the two sample areas, decreasing species' richness associated with increasing urban cover corresponds with reductions in the areas of a number of semi-natural habitats, hostplants and nectar sources. Despite these statistically significant correlations, the impact of urban cover on species' richness is weak. The maximum loss rate identified anywhere within the region is 0.81 species per 10% change in urban cover for South West Manchester. This finding may reflect on the generally low species diversity of the region. However, these results could be influenced by recording and sampling artefacts, particularly the failure of mapping programmes to distinguish vagrant individuals from breeding populations and a bias of records to vagrants. This is supported by the higher correlations between species' incidence and nectar sources than between species' incidence and their hostplants. Adult butterflies are opportunistic nectar users and nectar sources are more widely spread and thus less influenced by urban development than are specific butterfly hostplants. The finding may also reflect on the capacity of most of the butterfly species to breed successfully on tiny areas of hostplant existing within extensively built-up areas. Moreover, the capacity of butterfly species to persist by using small fragments of hostplants would be enhanced by vagrancy. If this is indeed the case, it is a finding that would support the value of small patches in butterfly metapopulations, albeit ones comprising incomplete complements of resources required during the life cycle. The incidence of most species decreases with increase in urban cover. Multivariate analyses indicate that this is owing to corresponding declines in hostplant-habitats and nectar sources. Five species increase with urban cover, but none attain formal significance. Associations among hostplants and habitat variables in a principal components analysis suggest that, in three cases (Pieris brassicae, P. rapae, Celastrina argiolus), this is owing to increasing areas of their hostplants within urban environments.     

Effects of food stress and density in different life stages on reproduction in a butterfly

Availability of adequate nutrition and (rearing) density are among the most important factors affecting growth, development and reproduction in animals. In holometabolous insects diets and energetic needs change between life stages, with storing of larval resources, adult feeding and reproduction being linked strategies. Nevertheless, studies investigating nutritional (and density) effects across metamorphic boundaries are largely lacking. We aim at disentangling the functional basis of reproductive patterns by independently manipulating larval and adult (1) density and (2) access to food, respectively, in the tropical butterfly, Bicyclus anynana. (1) A high larval rearing density had, contrary to common wisdom, very little impact on body size, but reduced larval development time through increased growth rates. The latter is thought to be an adaptation to high densities, driven by the risk of larval food resources becoming exhausted before reaching metamorphosis. Larval density and male company during oviposition (i.e. adult density) had no detectable effects on female reproduction. (2) Larval food stress prolonged larval development time and reduced larval growth rate, body size, fecundity and reproductive investment. Detrimental effects on female reproduction were mediated through a reduction in body size. Additional negative effects of adult food stress on fecundity were largely confined to females being fed as larvae ad libitum, while those being previously starved showed reduced performance regardless of adult income. Effects on egg size were inconsistent and, overall, marginal. Our results show that restricted food access in different developmental stages may set different limits to reproduction, either posed by shortage of larval‐derived storage reserves (i.e. nitrogenous compounds) or adult income (i.e. carbohydrates). Thus, one should be cautious when stating that one or the other type of nutrients is ultimately limiting to reproduction. Rather, our findings highlight the importance of resource congruence and of considering both, larval‐ and adult‐derived resources for reproduction.