Differential use of conspecific-derived information by sexual and asexual parasitic wasps exploiting partially depleted host patches

When foraging partially depleted patches (i.e., a fraction of hosts are already parasitized), female parasitoids must decide: 1—whether to superparasitize, and 2—whether to stay in their current patch (thus missing the opportunity of finding a better patch elsewhere). To make these decisions, parasitoids may rely on different cues, produced both by the environment and by conspecifics. Animals thriving in different environments may differ in cues they use. In the solitary parasitoid Venturia canescens, thelytokous (asexual) and arrhenotokous (sexual) individuals are found in two contrasting environments. Thelytokous females, from anthropogenic conditions, are known to cope with superparasitism in an adaptive way. On the other hand, little is known about superparasitism by arrhenotokous females. We compared the host exploitation strategies of thelytokous and arrhenotokous females in partially depleted patches. Hosts parasitized by thelytokous females were more frequently avoided than those parasitized by arrhenotokous females, suggesting a stronger chemical marking of the former. Only thelytokous females used information from conspecifics for patch-leaving decisions. The conformity of the differences in the behavior of thelytokous and arrhenotokous females with the environmental conditions they experience in their habitat is discussed.     

Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi

Summary In parasitoid wasps, self-superparasitism (oviposition into a host already parasitized by the female herself) often contributes less to the reproductive success of the parasitoid than oviposition into a host previously parasitized by a conspecific (conspecific superparasitism). It could therefore often be profitable for parasitoids to avoid self-superparasitism. This requires a mechanism for either (1) the avoidance of previously searched areas and/or (2) the rejection of hosts containing eggs laid by the searching female. We investigated whether the solitary parasitoid Epidinocarsis lopezi is able to avoid self-superparasitism. We show that visits to previously searched patches were shorter than visits to unsearched patches and conclude that E. lopezi females leave a trail odour on patches they have searched. No differences were found between the time on patches previously searched by the wasp itself and on patches visited by conspecifics. However, E. lopezi superparasitizes fewer hosts previously parasitized by itself than hosts parasitized by a conspecific. Thus, they recognize an individual-specific mark in or on the host. We discuss how patch marking and host marking enable E. lopezi to avoid self-superparasitism.     

Effects of within- and among-patch experiences on the patch-leaving decision rules in an insect parasitoid

The present study aimed to address how an insect parasitoid makes patch-departure decisions from various types of host patches and how previous patch experiences in the environment modify this decision-making process. Experiments were done with the parasitic wasp Aphidius rhopalosiphi attacking the grain aphid Sitobion avenae. In the experiments, wasps were observed in a laboratory environment containing several patches of various host densities, and behavioural records were analysed using a Coxs proportional hazards model. Consideration of the effect of the within-patch experience gave a classic pattern of patch-leaving decision rules in parasitoids: A. rhopalosiphi used local information on host quality (i.e. numbers of ovipositions or rejections) and availability (i.e. patch density) to determine departure decision. However, consideration of previous patch experiences provided evidence that these departure rules are fundamentally dynamic, responding to the physiological state of the animal and the information it has about its environment. Results showed that A. rhopalosiphi decreased its tendency to leave the visited patch after an oviposition. However, when a female has already laid several other eggs in the environment, such an incremental mechanism gradually switched to a decremental one. Hence, A. rhopalosiphi responded to egg-load depletion by leaving the visited patches sooner and by depositing a smaller number of eggs in those patches, which probably led to a decreased level of superparasitism. Results also indicated that previous experiences enabled wasps to estimate spatial host distribution and then to adjust their behavioural decisions accordingly. Thus, A. rhopalosiphi was shown to adjust its patch residence time according to the quality and the number of the patches previously visited. These proximate mechanistic rules adopted by A. rhopalosiphi females are discussed in the context of general predictions from optimality models.Communicated by D. Gwynne     

Patch leaving decision rules in parasitoids: do they use sequential decisional sampling?

Within the framework of optimal foraging theory, models assume that parasitoid insects are able to evaluate the quality of the patch in which they are currently searching for hosts and the travel time between patches. They can adjust their residence time in consequence. Simple and more realistic decision mechanisms that induce behavior compatible with the predictions of these models have been proposed for a number of species. Most of these decision mechanisms only take into account the presence of unparasitized hosts. Here, we studied the consequences for leaving patches containing different proportions of unparasitized and parasitized hosts. We support the hypothesis that parasitoids sample their environment and we propose a binomial sequential model, based on the type of host encountered (unparasitized or parasitized) instead of on the time spent in a patch, to explain the giving-up behavior of a parasitoid in a patch. A motivational incremental/decremental stochastic process is proposed to explain a possible mechanism of the apparent sampling scheme followed by the insect. The empirical data support the hypothesis of a sequential, decisional, binomial sampling scheme performed with a limited memory. This memory is, in fact, more an effect of habituation than the "true memory" of the parasitoid. The theoretical model was applied to real data obtained with an encyrtid parasitoid. These data were also compared to realizations of the incremental/decremental process.     

Dynamic response to danger in a parasitoid wasp

Despite the multitude of work on patch time allocation and the huge number of studies on patch choice in the face of danger, the patch leaving response of foragers perceiving cues of danger has received relatively little attention. We investigated the response of parasitoid insects to cues of danger both theoretically and experimentally. Using stochastic dynamic theory, we demonstrate that patch-leaving responses in response to the detection of danger should be seen as a dynamic decision that depends upon reproductive options on the current host patch and on alternative patches that might be found after leaving the current patch. Our theory predicts a sigmoidal response curve of parasitoids, where they should accept the danger and stay on the patch when patch quality is high and should increasingly avoid the risk and emigrate from the patch with decreasing patch quality and decreasing costs of traveling to an alternative host patch. Experiments with females of the drosophilid parasitoid Asobara tabida that were exposed to a puff of formic acid (a danger cue) at different times through their patch exploitation confirmed the theoretical predictions (i.e., a sigmoid response curve); however, the predicted curve was significantly steeper than observed. We discuss the impact of dynamic patch-exit decisions of individual foragers on population and community dynamics.     

Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms

As most parasitoids are time limited, they usually die before they have laid all their eggs. In such cases, optimal foraging theory predicts that female parasitoids will adopt behavioral reproductive strategies enabling them to maximize progeny production per unit of time. One key situation in which parasitoid females must optimize their time budget is related to the fact that most of their hosts are distributed in discrete patches in the environment. In this review, I first present the results of basic theoretical models predicting female wasp search duration on a patch of hosts. I then compile and analyze all studies investigating the effect of different factors on parasitoid patch time allocation and patch-leaving decision rules. Different patch-leaving mechanisms that were proposed to explain the results obtained are discussed, along with statistical methods that should be used to estimate them from experimental data. Finally, ideas for future research are presented.     

Specificity of odour-mediated avoidance of competition in Drosophila parasitoids

Although there are many examples of the role of volatile infochemicals in interactions between trophic levels of insect communities, surprisingly little is known of volatile interactions between species within the third trophic level. Recently it was found that Leptopilina heterotoma, an endoparasitoid that attacks Drosophila larvae, avoids one type of patches (decaying stinkhorn mushrooms) when parasitoids of another species (L. clavipes) are present on these patches. L. heterotoma is able to smell the presence of L. clavipes from a distance (Fig. 1). In this paper we investigate the source of the odour that induces avoidance behaviour, by varying the host species and parasitoid species present on stinkhorn mushrooms, and by using another type of patch (sap-fluxes of wounded trees). L. heterotoma was found to avoid stinkhorn patches with conspecific as well as heterospecific parasitoids (Fig. 2). Hosts had to be present in the patch to elicit avoidance, but avoidance behaviour was also found with another host species present in the patch (Fig. 3). No avoidance behaviour was found with sap-flux patches with hosts and parasitoids on them (Fig. 4). Avoidance of stinkhorn patches only occurred when the parasitoids present on the patch were able to contact hosts (Figs. 5 and 6). The exact source of the odour that elicits avoidance is still unclear, so that one can only speculate on the function of the signal. However, there is a clear benefit to the receiver, because it is able to avoid superior competitors. Avoidance can lead to non-aggregated parasitoid distributions. The importance of avoidance behaviour for population dynamics and stability of parasitoid-host systems is discussed.     

How temperature and habitat quality affect parasitoid lifetime reproductive success—A simulation study

Adult parasitoid females lay their eggs in or on host insects. Most species are incapable of de novo lipogenesis as adults, and lipids accumulated during the larval stage are allocated either to egg production or to adult survival. Lipid consumption increases with distance covered by the parasitoids and thus with the distance between available hosts within a habitat. Temperature should affect parasitoid fitness because it changes the constraint imposed by a limited reserve of lipids and because it influences behaviour. Climate change involves both an increase in average temperature and an increased frequency of extreme weather such as heat waves. We investigated how the predicted increase of temperature will affect parasitoid fitness and how this depends on habitat parameters (spatial distribution of hosts and lipid cost of habitat exploitation). We studied optimal behaviour and calculated fitness at different temperatures and in different habitats using a stochastic dynamic programming model for pro-ovigenic parasitoids (which mature all their eggs before becoming adult). We show that an increase in temperature decreases fitness of parasitoids adapted to lower temperatures. This decrease in fitness depends on habitat quality. In field conditions (assuming small costs of intra-patch foraging), the loss of fitness should be larger in habitats with high inter-patch distance and in habitats with a more aggregated distribution of hosts. The foraging behaviour of parasitoids is also affected; at higher temperature we show that intra-patch foraging becomes less efficient, and patch residence times are longer.     

The theoretical value of encounters with parasitized hosts for parasitoids

A female parasitoid searching for hosts in a patch experiences a diminishing encounter rate with unparasitized and thus suitable hosts. To use the available time most efficiently, it constantly has to decide whether to stay in the patch and continue to search for hosts or to search for and travel to another patch in the habitat. Several informational cues can be used to optimize the searching success. Theoretically, encounters with unparasitized hosts should lead to a prolonged search in a given patch if hosts are distributed contagiously. The results of empirical studies strongly support this hypothesis. However, it has, to date, not been investigated theoretically whether encounters with already parasitized hosts (which usually entail time costs) provide a parasitoid with valuable information for the optimization of its search in depletable patches, although the empirical studies concerning this question so far have produced ambiguous results. Building on recent advances in Bayesian foraging strategies, we approached this problem by modeling a priori searching strategies (which differ in the amount of information considered) and then testing them in computer simulations. By comparing the strategies, we were able to determine whether and how encounters with already parasitized hosts can yield information that can be used to enhance a parasitoid’s searching success.

Superparasitism and ovicide in parasitic Hymenoptera: theory and a case study of the ectoparasitoid Bracon hebetor

Summary Among insect parasitoids, superparasitism is said to occur when a second clutch of eggs is laid on a previously parasitized host. Ovicide occurs when a parasitoid destroys a clutch of eggs laid on a host by a previous female. Here, general models are constructed to predict the conditions which favor superparasitism and ovicide. Major predictions for the ovicidal model were that ovicide is more likely to occur if the time necessary to kill eggs is short, if travel times and the proportion of parasitized hosts increases and if the competitive advantage of a first clutch is large. The predictions of the models were tested by examining superparasitism and ovicide in Bracon hebetor (Say), a gregarious, ectoparasitoid of phytisiine moths. Using a wild and eye color mutant of B. hebetor to distinguish first and second clutches, it was found that the competitive advantage of a first clutch over a second clutch increased with the time between ovipositions. Patterns of superparasitism and ovicide in B. hebetor were in qualitative agreement with the major predictions of the model. Most notable, ovicide increased in frequency with a decrease in the overall rate of host encounter and an increase in the proportion of parasitized hosts encountered.     

Furanocoumarins and their detoxification in a tri-trophic interaction

The parsnip webworm, Depressaria pastinacella, specializes on wild parsnip, Pastinaca sativa, and several species of Heracleum, hostplants rich in toxic furanocoumarins. Rates of furanocoumarin metabolism in this species are among the highest known for any insect. Within its native range in Europe, webworms are heavily parasitized by the polyembryonic parasitoid wasp Copidosoma sosares. In this study, we determined whether these parasitoids are exposed to furanocoumarins in host hemolymph, whether they can metabolize furanocoumarins, and whether parasitism influences the ability of webworms to detoxify furanocoumarins. Hemolymph of webworms fed artificial diet containing 0.3 % fresh weight xanthotoxin, a furanocoumarin prevalent in wild parsnip hosts, contained trace amounts of this toxin; as well, hemolymph of webworms consuming P. sativa flowers and fruits contained trace amounts of six of seven furanocoumarins present in the hostplant. Thus, parasitoids likely encounter furanocoumarins in host hemolymph. Assays of xanthotoxin metabolism in C. sosares failed to show any ability to metabolize this compound. Parasitized webworms, collected from populations of Heracleum sphondylium in the Netherlands in 2004, were on average 55 % larger by weight than unparasitized individuals. This weight is inclusive of host and parasitoid masses. Absolute rates of detoxification (nmoles min⁻¹) of five different furanocoumarins were indistinguishable between parasitized and unparasitized ultimate instars, suggesting that the intrinsic rates of metabolism are fixed. Thus, although parasitized larvae are larger, detoxification rates are not commensurate with size; rates in parasitized larvae expressed per gram of larval mass were 25 % lower than in unparasitized larvae.     

Travel time affects optimal diets in depleting patches

Models of prey choice in depleting patches predict an expanding specialist strategy: Animals should start as specialists on the most profitable prey and then at some point during patch exploitation switch to a generalist foraging strategy. When patch residence time is long, the switch to a generalist diet is predicted to occur earlier than when patch residence time is short. We tested these predictions under laboratory conditions using female parasitoids (Aphidius colemani) exploiting patches of mixed instars aphid hosts (Myzus persicae, L1 and L4). The duration of patch exploitation was manipulated by changing travel time between patches. As predicted, patch residence times increase with travel time between patches. Our results provide empirical support for the expanding specialist prediction: Parasitoid females specialized initially on the more profitable hosts (L4), and as the patch depleted, they switched to a generalist diet by accepting more frequently the less profitable hosts (L1). The point at which they switched from specialist to generalist occurred later when travel times and hence patch residence times were short. By affecting the patch exploitation strategy, travel time also determines the composition of hosts left behind, the “giving up composition.” The change in the relative density of remaining host types alters aphid populations’ age structure.     

Learning and natal host influence host preference,handling time and sex allocation behaviour in a pupal parasitoid

The host choice and sex allocation decisions of a foraging female parasitoid will have an enormous influence on the life-history characteristics of her offspring. The pteromalid Pachycrepoideus vindemiae is a generalist idiobiont pupal parasitoid of many species of cyclorrhaphous Diptera. Wasps reared in Musca domestica were larger, had higher attack rates and greater male mating success than those reared in Drosophila melanogaster. In no-choice situations, na?ve female P. vindemiae took significantly less time to accept hosts conspecific with their natal host. Parasitoids that emerged from M. domestica pupae spent similar amounts of time ovipositing in both D. melanogaster and M. domestica. Those parasitoids that had emerged from D. melanogaster spent significantly longer attacking M. domestica pupae. The host choice behaviour of female P. vindemiae was influenced by an interaction between natal host and experience. Female P. vindemiae reared in M. domestica only showed a preference among hosts when allowed to gain experience attacking M. domestica, preferentially attacking that species. Similarly, female parasitoids reared on D. melanogaster only showed a preference among hosts when allowed to gain experience attacking D. melanogaster, again preferentially attacking that species. Wasp natal host also influenced sex allocation behaviour. While wasps from both hosts oviposited more females in the larger host, M. domestica, wasps that emerged from M. domestica had significantly more male-biased offspring sex ratios. These results indicate the importance of learning and natal host size in determining P. vindemiae attack rates, mating success, host preference and sex allocation behaviour, all critical components of parasitoid fitness. Electronic Publication     

Intraspecific hyperparasitism in a primary hymenopteran parasitoid

In solitary parasitoids, in which only one individual can emerge per host, the adaptive value of conspecific superparasitism is a function of the survival probability of the egg laid by the superparasitizing female. In the few cases which these probabilities are compared, the oldest immature has an advantage over the other individuals. We measured the acceptance rate of parasitized hosts and survival rate of supernumerary larvae in Anaphes victus (Hymenoptera: Mymaridae) in relation to the interval between ovipositions. When this interval was 5–7 days, the first immature was at the prepupa and pupa stage respectively, and female Anaphes victus changed their oviposition behavior markedly. They killed the developing parasitoid of their own species before ovipositing in it. The progeny of these females, which are normally primary parasitoids, developed thereafter as hyperparasitoids. Indeed, in contrast with other species, the survival of the second female's progeny increased with the time interval between ovipositions. This type of facultative intraspecific hyperparasitism is different from autoparasitism in Aphelinidae and has never been mentioned in other parasitoids; it would be adaptive if females of this short-lived species encounter low-quality patches.     

Precise sex allocation, local mate competition, and sex ratio shifts in the parasitoid wasp Trichogramma pretiosum

We determined the sex, order, and clutch size of eggs laid by the parasitoid wasp, Trichogramma pretiosum Riley, in the eggs of one of its natural hosts, Trichoplusia ni (Hübner). The parasitoid allocated sex non-randomly to hosts in the laboratory with a variance significantly less than that of a binomial (random) distribution, our null model. More clutches of two or more eggs contained a single male egg as the second or third egg laid than would be expected by chance and none contained two or more male eggs. T. pretiosum also increased the sex ratio (% male) of its offspring with increasing foundress numbers by increasing the frequency of male offspring as the second egg in a two-egg clutch allocated to unparasitized hosts and as the single egg allocated to previously parasitized hosts. These results indicate that T. pretiosum allocates the sex of its offspring precisely. Precise sex allocation is favored under local mate competition because it reduces variation in the number of sons per patch thus maximizing the number of inseminated daughters emigrating from the patch. Similar combinations of female and male offspring emerged from T. ni eggs parasitized by T. pretiosum in the field, again with a sex ratio variance less than that expected for a binomial distribution. These results strongly suggest that this parasitoid species manifests local mate competition.     

Travel duration,energetic expenditure,and patch exploitation in the parasitic wasp <Emphasis Type="Italic">Venturia canescens</Emphasis>

Foraging animals usually keep track of how costly it is to reach new resource patches and adjust patch residence time and exploitation rate accordingly. There are at least two potential factors, which are not necessarily closely linked, that animals could measure to estimate costs of traveling: the time the forager needs to reach the next patch and the amount of energy it has to invest until arrival. In the parasitoid wasp Venturia canescens, females forage for hosts from which their offspring can develop. Two different types of this parasitoid exist. The thelytokous type lives in anthropogenic habitats where flight is not necessarily linked with foraging. The arrhenotokous type lives under field conditions and shows frequent flight activity. We tested whether the wasps would use time or energy needed to assess patch availability, by either confining them into vials or letting them travel actively in a flight mill between patch visits. Our results show that in thelytokous lines, time is a sufficient cue influencing patch exploitation and an additional effect of the energy needed was not visible. In the arrhenotokous wasps, however, only the number of rounds flown in the mill influenced subsequent behavior, while mere time spent traveling did not. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Different habitats, different habits? Response to foraging information in the parasitic wasp Venturia canescens

The parasitic wasp, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), has two reproductive modes, namely, thelytoky or arrhenotoky, and occurs in habitats with highly variable or relatively stable host abundances, respectively. Since information processing is costly, we expected that information indicating resource availability would be mainly used by the thelytokous wasps and less so by the arrhenotokous type. This idea was explored by two different approaches. In a study on patch-time allocation, we used females from ten populations and measured patch-residence times of individuals that visited multiple patches at different encounter rates. In a more detailed approach, thelytokous and arrhenotokous females from a single location were observed continuously while foraging, and all behaviors were recorded. Wasps of both reproductive modes (i.e., both habitat types) used information for the assessment of habitat quality. However, the way that the information was used differed between them. Whereas thelytokous females used foraging information to maximize their efficiency at high patch-encounter rates, arrhenotokous females merely reduced the number of offspring produced without changing patch times. The behavior of the arrhenotokous females should result in a spreading of offspring across the habitat and, thus, reduced sib-mating. The foraging strategy of these wasps might therefore be an adaptation to reduce costs associated with inbreeding.     

Adaptive responses to local mate competition by the parasitoid,Telenomus remus

Summary The parasitic wasp, Telenomus remus, lays her eggs in diserete patches of moth eggs, where her offspring develop and mate before dispersal, satisfying conditions for local mate competition (LMC). In the presence of other ovipositing females, wasps lay a higher sex ratio (proportion males), as predicted by LMC theory, and achieve this by a combination of two mechanisms, (1) avoidance of superparasitism and a sequence of sex allocation initially biased towards males and (2) a direct increase in sex ratio in the presence of other wasps, sex ratio increases with the proportion of previously parasitized hosts, as predicted by LMC theory. In both cases, chemical traces left by foraging wasps are indicated as the stimuli causing wasps to increase the proportion of males allocated to hosts.     

The relationship between conspecific superparasitism and the outcome of in vitro contests staged between different larval instars of the solitary endoparasitoid Venturia canescens

When endoparasitoid wasps oviposit into hosts which have already been parasitized (= superparasitism), this results in potentially lethal interlarval competition. For solitary species, the decision to lay additional eggs should therefore be based on the probability of superparasite survival in any superparasitized host. In this study, in vitro contests staged between three larval instars of Venturia canescens Grav. (Hymenoptera: Ichneumonidae) reveal that the age difference between competitors affects the outcome of interlarval competition. Three parameters were used to assess parasitoid performance: the number of fights initiated, the number of bites inflicted, and the duration of each bite. When fighting takes place between two first instars, then both competitors were found to be evenly matched. However, at greater age differences, first-instar competitors appeared to win more fights than their larger second instar rivals. The advantage shown by younger competitors is most pronounced in contests staged between first and third instar larvae. These findings are consistent with the increasingly high levels of conspecific superparasitism shown by V. canescens in the first 5 days after initial host attack, suggesting that this parasitoid can deploy her use of deliberate superparasitism in an adaptive way. Received: 13 December 1995/Accepted after revision: 5 March 1996     

Searching behavior and use of sampling information by free-ranging bison (Bos bison)

I examined the searching behavior of free-ranging plains bison (Bos bison bison) in their natural habitat, and determined whether their assessment of food patch quality was influenced by the short-term sampling information acquired during search. Bison used area-concentrated search during their winter foraging activity. Their movements between areas of suitable food patches were influenced by local environmental conditions, being sometimes less sinuous, and at other times more sinuous, than expected from a correlated random walk model. Bison also systematically avoided digging in areas where plants of low profitability lay under the snow. Where they dug, there was evidence that a bison's perception of food quality varied during a foraging bout, and was therefore influenced by short-term sampling information. After controlling for forage quality, I found that small feeding craters were more likely to be preceded by samples of high quality food patches. My observations suggest that bison take advantage of the structural characteristics of their environment during searching activity, and base foraging decisions on local rather than global availability.