Emmanuel Desouhant

Energy dynamics in a parasitoid foraging in the wild

Although parasitoids are used widely as a biological models for understanding the evolution of animal behaviour, most studies have been constrained to the laboratory. The dearth of field studies has been compounded by the almost complete ignorance of the physiological parameters involved in foraging and dispersal, in particular of the energetic constraints imposed by resource limitation. We estimated the dynamics of carbohydrates and lipids reserves of Venturia canescens (Gravenhorst) females by releasing individuals of known nutritional status in a natural environment and recapturing them using host-containing traps. The recapture rate was around 30%. These results were compared with the reserves of caged animals kept under different experimental conditions (freshly emerged, starved to death, fed ad libitum and partially starved). Wild animals were also sampled in order to estimate the resource levels of the local population. The results show that: (i) wasps are able to maintain a nearly constant level of energy over an extended foraging period; (ii) V. canescens takes sugars in the field; and (iii) the lipid reserves accumulated during the larval life may be limiting as lipogenesis does not take place in adults even under conditions of high sugar availability. These results demonstrate that wasps can forage for hosts and food and disperse in this habitat for hours and days without running into a severe risk of energy limitation.

Host and food searching in a parasitic wasp Venturia canescens : a trade-off between current and future reproduction?

Whether to invest in current or future reproduction is an important trade-off in life history evolution. For insect parasitoids, this trade-off is determined, among other factors, by the decision whether to search for hosts (immediate gain of fitness) or food (delayed fitness gains). Although host searching has been well studied, food sources, cues that parasitoids use to search for food and how insects modify their feeding behaviour have not. To address these questions, we investigated the food- and host-searching decisions made by the parasitoid Venturia canescens in both laboratory (olfactometer experiments) and field conditions (choice experiments). The wasps detected chemical cues associated with food, as well as those associated with hosts, and moved towards one or the other according to their nutritional state. Females used as food sources the same fruits that harboured hosts and detected the olfactory cues that would direct them to these fruits. Field results were consistent with those obtained in the laboratory. By integrating responses to infochemicals related to host and food, V. canescens might reduce the costs associated with food searching, so that more time and energy can be allocated to foraging for hosts. This behaviour should result in an adaptive advantage over parasitoids that incur additional costs by searching for hosts and food in different locations.

Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause

Abstract. Diversified bet-hedging for life cycle duration is defined as within-generation variability in cycle length expressed by a single genotype maximising mean geometric fitness. Such plasticity is not predictive, i.e. it is not a response to cues from the environment that has a predictive value for the decision at hand. In evolutionary terms, diversified bet-hedging is perceived as an adaptation to environmental stochasticity. However, clear evidence of bet-hedging is scarce and exists only for a few desert plant species and one desert bee. In temperate insects, diversified bet-hedging for life cycle duration has been suspected in the chestnut weevil, but proximate factors responsible for individual variation are still unknown. From field experiments, we show that the frequency of the long cycle depends on larval weight and on the date when a larva abandons the fruit, but not on larval burying depth in the soil. Since the two first factors are known to depend on food and temperature and cannot lead to predictive plasticity, we give evidence of bet hedging in this temperate species. Indeed, despite a cost associated with prolonged diapause (extra mortality and loss of reproductive opportunity), a previous study showed that plasticity for life cycle duration, such as discussed in this paper, maximises mean geometric fitness and persistence probability in the chestnut weevil. We propose the hypothesis that the variation in life cycle duration depends on individual variability of metabolic resources such as lipids.

The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.

Differential energy allocation as an adaptation to different habitats in the parasitic wasp Venturia canescens

Environmental pressures are expected to favour organisms that optimally allocate metabolic resources to reproduction and survival. We studied the resource allocation strategies and the associated tradeoffs in the parasitoid wasp Venturia canescens, and their adaptation to the characteristics of the environment. In this species, individuals of two reproductive modes coexist in the same geographical locations, but they mainly occur in distinct habitats. Thelytokous (asexual) wasps are mostly found in anthropogenic habitats, where hosts tend to aggregate and food is absent. Arrhenotokous (sexual) wasps are exclusively found in natural habitats, where hosts are scattered and food is present. We analysed (1) the quantity of energy stored during ontogeny, (2) the tradeoff between reproduction and survival, by measuring egg load and longevity and (3) the host patch exploitation behaviour of the wasps at emergence. Arrhenotokous wasps emerged with more metabolic resources than thelytokous ones, especially glycogen, a nutrient that could be used for flying in search of hosts and/or food. Thelytokous wasps allocated more energy than arrhenotokous wasps to egg production: this would allow them to parasitize more hosts. The tradeoff between egg production and longevity was not revealed within reproductive modes, but when comparing them. At emergence, arrhenotokous wasps tended to exploit host patches less thoroughly than thelytokous wasps, suggesting that by leaving the host patch, they search for food. The results clearly showed adaptations to the characteristics of habitats preferentially inhabited by the two reproductive modes, and suggested a mechanism that facilitates their coexistence in natural conditions.

A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited

Insects comprise relevant biological models for investigating nutrient acquisition and allocation processes in the context of life‐history ecology and evolution. However, empirical investigations are still partly limited by the lack of availability of simple methods for simultaneously estimating the four major energetic components (i.e. lipids, free sugars, glycogen and proteins) in the same individual. In the present work, we validate a fast, reproducible and cheap method for overcoming this problem that uses different solvents successively. First, proteins are solubilized in a phosphate‐lysis buffer and then quantified according to the classical Bradford assay procedure. In a second step, a chloroform–methanol mixture is added to the aqueous phase, which allows assay of the total lipid fraction, as well as the free sugars and glycogen in the same insect homogenate. In addition, a micro‐separation procedure is adapted to partition the total lipids into neutral (mainly stored lipids) and polar (mainly structural lipids) components. Although these assays are conducted sequentially in the same individual, the sensitivity of our method remains high: the estimated amount of each energetic compartment does not differ from that obtained with former, partial methods. Our method should thus largely improve our knowledge about nutrient acquisition and allocation among insects not only in laboratory‐reared individuals, but also in animals caught in the wild. Descriptions and recommendations are given at each step of the protocol to adapt the procedure to various insect species. Finally, to prevent misinterpretation of data generated in accordance with this protocol, the limits of our method are discussed in the light of life‐history studies.

Clutch size manipulations in the chestnut weevil, Curculio elephas: fitness of oviposition strategies

Abstract We test the adaptive value of clutch size observed in a natural population of the chestnut weevil Curculio elephas. Clutch size is defined as the number of immatures per infested chestnut. In natural conditions, clutch size averages 1.7 eggs. By manipulating clutch size in the field, we demonstrate that deviations from the theoretical ”Lack clutch size”, estimated as eight immatures, are mainly due to proximate and delayed effects of clutch size on offspring performance. We show the existence of a trade-off between clutch size and larval weight. The latter, a key life-history trait, is highly correlated with fitness because it is a strong determinant of larval survival and potential fecundity of offspring females. The fitness of different potential oviposition strategies characterized by their clutch sizes, ranging from one to nine immatures, was calculated from field- estimated parameters. Chestnut weevil females obtain an evolutionary advantage by laying their eggs singly, since, for instance, fitness of single-egg clutches exceeds fitness of two-egg clutches and four-egg clutches by 8.0% and 15.1% respectively.

Dispersal between host populations in field conditions: navigation rules in the parasitoid Venturia canescens.

Abstract. 1. Dispersal is a life‐history trait that can have great ecological and evolutionary consequences, however understanding of how insects disperse is limited.

Selection of fruits for oviposition by the chestnut weevil, Curculio elephas

Under field conditions, females of the chestnut weevil Curculio elephas select their oviposition sites. In sleeve experiments, when the number of fruits is limited, females avoid 17% of available chestnuts and concentrate their eggs in the others. In the field, on average, 56.3 and 27.8% of the infested fruits contain one or two immatures (eggs and larvae). The oviposition site selection is neither influenced by host size nor by the presence of immature conspecifics. Choice experiments in the laboratory suggest that female weevils do not deposit repellent chemical markers on the fruits. Moreover, sleeve experiments indicate that selection is not influenced by the noise made by larvae while feeding inside a fruit. In general, the most probable hypothesis is that Curculio elephas exploits only hosts of highest feeding quality.

Impact of Wolbachia on oxidative stress sensitivity in the parasitic wasp Asobara japonica

The oxidative homeostasis is the balance between reactive oxygen species and antioxidant molecules. In addition to be considered as a key factor underlying life-history traits evolution, the oxidative homeostasis has been shown to be involved in many host–symbiont associations. Previous studies suggest an interaction between the bacterial endosymbiont Wolbachia and the oxidative homeostasis of some insect hosts. This interaction is likely to exert a strong influence on the host evolution, as it has been proposed in the wasp Asobara tabida, whose dependence upon Wolbachia is due to the evolutionary loss of its ability to regulate the oxidative homeostasis in the absence of the symbiont. Although such cases of complete dependence are rare, cases of insects having lost only a part of their autonomy over the control of the oxidative homeostasis might be more common. If so, one can expect that insects having coevolved with Wolbachia will be more sensitive to oxidative stress when cured of their symbionts. We tested this hypothesis by studying the effects of an experimentally-induced oxidative stress on various life-history traits of Asobara japonica, a species closely related to A. tabida. For most of the life-history traits studied, the sensitivity of the wasps to oxidative stress did not correlate with their infection status. The only exception was the parasitic success. However, contrarily to our expectation, the sensitivity to oxidative stress was increased, rather than decreased, when Wolbachia was present. This result suggests that Wolbachia does not participate to mitigate oxidative stress in A. japonica, and that on the contrary its presence might still be costly in stressful environments.